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A Longitudinal Metagenomic Comparative Analysis of Oral Microbiome Shifts in Patients Receiving Proton Radiation versus Photon Radiation for Head and Neck Cancer Cover

A Longitudinal Metagenomic Comparative Analysis of Oral Microbiome Shifts in Patients Receiving Proton Radiation versus Photon Radiation for Head and Neck Cancer

Journal of Cancer and Allied Specialties
Volume 10 (2024): Issue 1 (January 2024)
By: Timothy F. Meiller,  Claire M. Fraser,  Silvia Grant-Beurmann,  Mike Humphrys,  Luke Tallon,  Lisa D. Sadzewicz,  Mary Ann Jabra-Rizk,  Areej Alfaifi,  Anmar Kensara,  Jason K. Molitoris,  Matthew Witek,  William S. Mendes,  William F. Regine,  Phuoc T. Tran,  Robert C. Miller and  Ahmed S. Sultan  
Open Access
|Jan 2024

Figures & Tables

Figure 1:

(a) Oral microbial taxa relative abundance differences between healthy, no radiation, photon, and proton radiation treatment recipients. Relative abundances of oral microbial taxa between photon and proton radiation recipients were measured pre-radiation exposure (PRE), during radiation treatment (r), and post-radiation exposure (POST). Veillonella, Streptococcus, Neisseria, and Actinomyces were more abundant in patients during proton radiation recipients, whereas Lymphocryptovirus, Lactobacillus, Capnocytophaga were the taxa that were more abundant in patients during photon radiation recipients. (b) Oral alpha diversity (observed species richness) for healthy, no radiation, oral inflammatory, photon, and proton radiation treatment recipients. Alpha diversity between photon and proton radiation recipients. Age and sex matched healthy controls (orange), head and neck cancer control without radiation therapy (lime green), oral inflammatory disease without radiation therapy (green), conventional photon radiation therapy (blue), proton radiation therapy (pink). C: Healthy controls, PRE: Baseline sample collection pre-radiation, R: Sample collection during radiation, POST: Sample collection immediately following the completion of radiation. No significant difference was observed between the treatments and timepoints (P > 0.05). (c) Oral alpha diversity (Chao1) for healthy, no radiation, oral inflammatory, photon, and proton radiation treatment recipients. Alpha diversity between photon and proton radiation recipients was measured PRE, during radiation treatment (r), and POST. No significant difference was observed between the treatments and timepoints (P > 0.05). (d) Shannon alpha diversity for healthy, no radiation, oral inflammatory, photon, and proton radiation treatment recipients. No significant shifts in diversity were observed across timepoints: PRE, R, POST
(a) Oral microbial taxa relative abundance differences between healthy, no radiation, photon, and proton radiation treatment recipients. Relative abundances of oral microbial taxa between photon and proton radiation recipients were measured pre-radiation exposure (PRE), during radiation treatment (r), and post-radiation exposure (POST). Veillonella, Streptococcus, Neisseria, and Actinomyces were more abundant in patients during proton radiation recipients, whereas Lymphocryptovirus, Lactobacillus, Capnocytophaga were the taxa that were more abundant in patients during photon radiation recipients. (b) Oral alpha diversity (observed species richness) for healthy, no radiation, oral inflammatory, photon, and proton radiation treatment recipients. Alpha diversity between photon and proton radiation recipients. Age and sex matched healthy controls (orange), head and neck cancer control without radiation therapy (lime green), oral inflammatory disease without radiation therapy (green), conventional photon radiation therapy (blue), proton radiation therapy (pink). C: Healthy controls, PRE: Baseline sample collection pre-radiation, R: Sample collection during radiation, POST: Sample collection immediately following the completion of radiation. No significant difference was observed between the treatments and timepoints (P > 0.05). (c) Oral alpha diversity (Chao1) for healthy, no radiation, oral inflammatory, photon, and proton radiation treatment recipients. Alpha diversity between photon and proton radiation recipients was measured PRE, during radiation treatment (r), and POST. No significant difference was observed between the treatments and timepoints (P > 0.05). (d) Shannon alpha diversity for healthy, no radiation, oral inflammatory, photon, and proton radiation treatment recipients. No significant shifts in diversity were observed across timepoints: PRE, R, POST

Figure 2:

(a) Pyrimidine deoxyribonucleotides de novo biosynthesis superpathway (PWY-7211). PWY-7211 was comparatively higher after photon exposure. No significant difference was observed between the treatments and timepoints (P > 0.05). (b) Nitrate reduction V pathway. The nitrate reduction pathway was upregulation during photon treatment. No significant difference was observed between the treatments and timepoints (P > 0.05)
(a) Pyrimidine deoxyribonucleotides de novo biosynthesis superpathway (PWY-7211). PWY-7211 was comparatively higher after photon exposure. No significant difference was observed between the treatments and timepoints (P > 0.05). (b) Nitrate reduction V pathway. The nitrate reduction pathway was upregulation during photon treatment. No significant difference was observed between the treatments and timepoints (P > 0.05)

Figure 3:

Oral complications and clinical correlates. Oral complications were determined by a board-certified oral medicine specialist (TFM), calibrated for the assessment of oral mucositis, salivary hypofunction, and fungal overgrowth with the assistance of a PhD mycologist (MAJ-R) that assessed all fungal characterization. The World Health Organization oral mucositis assessment scale was used for oral mucositis determination. Each assessment was made prior to the onset of therapy, midpoint of therapy, and at the endpoint. Saliva collections were timed to assess volumetric salivary hypofunction, coupled with culturing to determine the presence of fungal species, determined to be either carriage or infection. Mucositis was observed in 3 out 4 photon patients during radiation therapy (r) and mucositis persisted to the end of therapy (POST). No mucositis was observed in any of the proton patients during radiation therapy (r) but mucositis was observed in 1/4 patients at the end of therapy (POST). Oral candidiasis was observed in 2 out 4 photon patients and in 1 out 4 proton patients during radiation therapy (r). Oral candidiasis persisted to the end of therapy (POST) in 2 photon patients. Xerostomia occurred in all patients except for 1 proton patient. Salivary hypofunction only occurred in one photon patient at the end of therapy (POST)
Oral complications and clinical correlates. Oral complications were determined by a board-certified oral medicine specialist (TFM), calibrated for the assessment of oral mucositis, salivary hypofunction, and fungal overgrowth with the assistance of a PhD mycologist (MAJ-R) that assessed all fungal characterization. The World Health Organization oral mucositis assessment scale was used for oral mucositis determination. Each assessment was made prior to the onset of therapy, midpoint of therapy, and at the endpoint. Saliva collections were timed to assess volumetric salivary hypofunction, coupled with culturing to determine the presence of fungal species, determined to be either carriage or infection. Mucositis was observed in 3 out 4 photon patients during radiation therapy (r) and mucositis persisted to the end of therapy (POST). No mucositis was observed in any of the proton patients during radiation therapy (r) but mucositis was observed in 1/4 patients at the end of therapy (POST). Oral candidiasis was observed in 2 out 4 photon patients and in 1 out 4 proton patients during radiation therapy (r). Oral candidiasis persisted to the end of therapy (POST) in 2 photon patients. Xerostomia occurred in all patients except for 1 proton patient. Salivary hypofunction only occurred in one photon patient at the end of therapy (POST)

Patient characteristics of study cohorts

Patient characteristicIMRT (n=4)IMPT (n=4)
Mean age (range)67 years (60–72)62 years (54–77)
Male sex (percentage)4 (100)4 (100)
Caucasian race3 (75)4 (100)
Current cigarette smoking3 (75)2 (50)
Chemotherapy2 (50)2 (50)
Surgery2 (50)0 (0)
Histology4 (100) SCC4 (100) SCC
Tumor site1 (25) Glossotonsillar1 (25) Base of tongue1 (25) Tonsil/Base of tongue1 (25) Supraglottic1 (25) Glossotonsillar3 (75) Tonsil
HPV status2 (50) Positive2 (50) Not performed4 (100) Positive
Radiation parameters
Prescription dose2 (50) 69.96 Gy2 (50) 60 Gy4 (100) 69.96 Gy
Dose/fraction2 (50) 2.12 Gy2 (50) 2 Gy4 (100) 2.12 Gy
1 Fractions/day4 (100)4 (100)
Parotid total mean dose (range)32.09 Gy (26.69–40.9)23.96 Gy (21.31–29.7)
Oral cavity total mean dose (range)41.01 Gy (28.87–61.11)19.59 Gy (15.6–25.43)
DOI: https://doi.org/10.37029/jcas.v10i1.579 | Journal eISSN: 2411-989X
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Language: English
Page range: 1 - 9
Submitted on: Aug 24, 2023
Accepted on: Dec 1, 2023
Published on: Jan 23, 2024
Published by: Shakuat Khanum Memorial Cancer Hospital and Research Centre
In partnership with: Paradigm Publishing Services
Publication frequency: 2 issues per year
Keywords:
Head and Neck Cancer,
metagenome,
oral microbiome,
radiation therapy
Related subjects:
Medicine,
Clinical medicine,
Internal medicine,
Internal medicine, other,
Haematology, oncology,
Pediatrics and juvenile medicine,
Paediatric haematology and oncology,
Surgery,
Surgery, other

© 2024 Timothy F. Meiller, Claire M. Fraser, Silvia Grant-Beurmann, Mike Humphrys, Luke Tallon, Lisa D. Sadzewicz, Mary Ann Jabra-Rizk, Areej Alfaifi, Anmar Kensara, Jason K. Molitoris, Matthew Witek, William S. Mendes, William F. Regine, Phuoc T. Tran, Robert C. Miller, Ahmed S. Sultan, published by Shakuat Khanum Memorial Cancer Hospital and Research Centre
This work is licensed under the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License.

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