Transitions in oral and gut microbiome of HPV+ oropharyngeal squamous cell carcinoma following definitive chemoradiotherapy (ROMA LA-OPSCC study)

Oliva, Marc; Schneeberger, Pierre H. H.; Rey, Victor; Cho, Matthew; Taylor, Rachel; Hansen, Aaron Richard; Taylor, Kenneth W.; Bayley, Andrew; Hope, Andrew; Bratman, Scott V.; Ringash, Jolie; Singh, Simron; Weinreb, Ilan; Perez-Ordoñez, Bayardo; Waldron, John; Xu, Wei; Guttman, David S.; Siu, Lillian L.; Coburn, Bryan; Spreafico, Anna

doi:10.1038/s41416-020-01253-1

Cited by 32 publications

(17 citation statements)

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“…An increased number and diversity of fungi, in addition to Candida , have been detected (e.g., Peniophora, Stereum, Cladosporium ) ( 3 ). The total number of bacteria tends to decrease immediately after treatment and gradually return, while the relative abundance of certain species (e.g., Streptococcus mutans ) and genera (e.g., Bifidobacterium, Lactobacillus) tend to increase and reflect gut-associated obligate anaerobes ( 3 , 27 , 28 , 33 , 35 ). Regarding archea, there seems to be little to no change due to RT ( 3 ).…”

Section: Radiation Therapy and Changes In The Head And Neck Microbiomementioning

confidence: 99%

“…The studies we present have methodological advantages over culture-based techniques: superior sensitivity, specificity, and speed in detecting microorganisms that may be responsible for causing RT-induced toxicity ( 39 , 66 ). By using “sequencing by synthesis” methods that target the 16S rRNA subunit ( 67 ), studies in this review allow for identification of microorganisms at the phyla and genera levels, while one study ( 33 ) used metagenomic shotgun sequencing to capture species-level changes. Recent advancements in molecular processing have made possible the use of a multi-omic approach—metagenomics, metabolomics, metatranscriptomics, and metaproteomics ( 68 )—to identify strain-level microorganisms and obtain additional information on how the microbiome may be related to clinical changes in the host ( 27 , 69 ).…”

Section: Future Directionsmentioning

confidence: 99%

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The Effect of Radiation and Chemoradiation Therapy on the Head and Neck Mucosal Microbiome: A Review

et al. 2021

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Radiation (RT) and chemoradiation therapy (CRT) play an essential role in head and neck cancer treatment. However, both cause numerous side effects in the oral cavity, paranasal sinuses, and pharynx, having deleterious consequences on patients’ quality of life. Concomitant with significant advances in radiation oncology, much attention has turned to understanding the role of the microbiome in the pathogenesis of treatment-induced tissue toxicity, to ultimately explore microbiome manipulation as a therapeutic intervention. This review sought to discuss current publications investigating the impact of RT and CRT-induced changes on the head and neck microbiome, using culture-independent molecular methods, and propose opportunities for future directions. Based on 13 studies derived from a MEDLINE, EMBASE, and Web of Science search on November 7, 2021, use of molecular methods has uncovered various phyla and genera in the head and neck microbiome, particularly the oral microbiome, not previously known using culture-based methods. However, limited research has investigated the impact of RT/CRT on subsites other than the oral cavity and none of the studies aimed to examine the relationship between the head and neck microbiome and treatment effectiveness. Findings from this review provide helpful insights on our current understanding of treatment-induced oral mucositis, dental plaque, and caries formation and highlight the need for future research to examine the effect of RT/CRT on the sinonasal and oropharyngeal microbiome. In addition, future research should use larger cohorts, examine the impact of the microbiome on treatment response, and study the effect of manipulating the microbiome to overcome therapy resistance.

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Section: Radiation Therapy and Changes In The Head And Neck Microbiomementioning

confidence: 99%

Section: Future Directionsmentioning

confidence: 99%

The Effect of Radiation and Chemoradiation Therapy on the Head and Neck Mucosal Microbiome: A Review

et al. 2021

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“…This study was positively classified in our LitSuggest analysis ( Table 3 ). A study by Oliva et al (2021) found that Leptotrichia hofstadii was abundant in stage III oropharynx cancer, while Zakrzewski et al (2021) determined Leptotrichia genus to be decreased in oropharynx HPV- tumor samples.…”

Section: Discussionmentioning

confidence: 99%

Haemophilus pittmaniae and Leptotrichia spp. Constitute a Multi-Marker Signature in a Cohort of Human Papillomavirus-Positive Head and Neck Cancer Patients

et al. 2022

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ObjectivesHuman papillomavirus (HPV) is a known etiological factor of oropharyngeal head and neck cancer (HNC). HPV positivity and periodontal disease have been associated with higher HNC risk, suggesting a role for oral bacterial species. Our objective was to determine oral microbiome profiles in HNC patients (HPV-positive and HPV-negative) and in healthy controls (HC).MethodsSaliva samples and swabs of buccal mucosa, supragingival plaque, and tongue were collected from HNC patients (N = 23 patients, n = 92 samples) before cancer therapy. Next-generation sequencing (16S-rRNA gene V3–V4 region) was used to determine bacterial taxa relative abundance (RA). β-Diversities of HNC HPV+ (N = 16 patients, n = 64 samples) and HNC HPV– (N = 7 patients, n = 28 samples) groups were compared using PERMANOVA (pMonte Carlo < 0.05). LEfSe discriminant analysis was performed to identify differentiating taxa (Log LDA > 2.0). RA differences were analyzed by Mann–Whitney U-test (α = 0.05). CombiROC program was used to determine multi-marker bacterial signatures. The Microbial Interaction Network Database (MIND) and LitSuggest online tools were used for complementary analyses.ResultsHNC vs. HC and HNC HPV+ vs. HNC HPV– β-diversities differed significantly (pMonte Carlo < 0.05). Streptococcus was the most abundant genus for HNC and HC groups, while Rothia mucilaginosa and Haemophilus parainfluenzae were the most abundant species in HNC and HC patients, respectively, regardless of antibiotics treatment. LEfSe analysis identified 43 and 44 distinctive species for HNC HPV+ and HNC HPV– groups, respectively. In HNC HPV+ group, 26 periodontal disease-associated species identified by LefSe had a higher average RA compared to HNC HPV– group. The significant species included Alloprevotella tannerae, Fusobacterium periodonticum, Haemophilus pittmaniae, Lachnoanaerobaulum orale, and Leptotrichia spp. (Mann–Whitney U-test, p < 0.05). Of 43 LEfSe-identified species in HPV+ group, 31 had a higher RA compared to HPV– group (Mann–Whitney U-test, p < 0.05). MIND analysis confirmed interactions between Haemophilus and Leptotrichia spp., representing a multi-marker signature per CombiROC analysis [area under the curve (AUC) > 0.9]. LitSuggest correctly classified 15 articles relevant to oral microbiome and HPV status.ConclusionOral microbiome profiles of HNC HPV+ and HNC HPV– patients differed significantly regarding periodontal-associated species. Our results suggest that oral bacterial species (e.g., Leptotrichia spp.), possessing unique niches and invasive properties, coexist with HPV within HPV-induced oral lesions in HNC patients. Further investigation into host–microbe interactions in HPV-positive HNC patients may shed light into cancer development.

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“…Oropharyngeal swabs and stool samples were collected from a cohort of patients with human papillomavirus-positive (HPV + ) locoregionally advanced oropharyngeal squamous cell carcinoma (LA-OPSCC) treated with chemoradiotherapy (CRT) ( 13 ). Oropharyngeal swabs over the tumor site and stool samples were collected up to 3 weeks prior to the start of radiotherapy and again at completion of CRT (up to 3 weeks following last day of radiotherapy) ( 13 ). Oropharyngeal swabs over the tumor site and stool samples were collected using the ZymoBIOMICS DNA/RNA mini prep kits (Zymo Research, Irvine, CA).…”

Section: Methodsmentioning

confidence: 99%

“…Oropharyngeal swabs over the tumor site and stool samples were collected using the ZymoBIOMICS DNA/RNA mini prep kits (Zymo Research, Irvine, CA). DNA was extracted using ZymoBIOMICS DNA micro kit ( 13 ).…”

Section: Methodsmentioning

confidence: 99%

Two-Target Quantitative PCR To Predict Library Composition for Shallow Shotgun Sequencing

et al. 2021

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Transitions in oral and gut microbiome of HPV+ oropharyngeal squamous cell carcinoma following definitive chemoradiotherapy (ROMA LA-OPSCC study)

Cited by 32 publications

References 34 publications

The Effect of Radiation and Chemoradiation Therapy on the Head and Neck Mucosal Microbiome: A Review

The Effect of Radiation and Chemoradiation Therapy on the Head and Neck Mucosal Microbiome: A Review

Haemophilus pittmaniae and Leptotrichia spp. Constitute a Multi-Marker Signature in a Cohort of Human Papillomavirus-Positive Head and Neck Cancer Patients

Two-Target Quantitative PCR To Predict Library Composition for Shallow Shotgun Sequencing

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