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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

Timothy F. Meiller

Timothy F. Meiller

  • Department of Oncology and Diagnostic Sciences, School of Dentistry, University of MarylandBaltimore, United States
  • University of Maryland Marlene and Stewart Greenebaum Comprehensive Cancer CenterBaltimore, United States
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Meiller, Timothy F.
, 
Claire M. Fraser

Claire M. Fraser

  • Department of Medicine, University of Maryland School of MedicineBaltimore, United States
  • Institute for Genome Sciences, University of Maryland School of MedicineBaltimore, United States
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Fraser, Claire M.
, 
Silvia Grant-Beurmann

Silvia Grant-Beurmann

Institute for Genome Sciences, University of Maryland School of MedicineBaltimore, United States
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Grant-Beurmann, Silvia
, 
Mike Humphrys

Mike Humphrys

Institute for Genome Sciences, University of Maryland School of MedicineBaltimore, United States
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Humphrys, Mike
, 
Luke Tallon

Luke Tallon

Institute for Genome Sciences, University of Maryland School of MedicineBaltimore, United States
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Tallon, Luke
, 
Lisa D. Sadzewicz

Lisa D. Sadzewicz

Institute for Genome Sciences, University of Maryland School of MedicineBaltimore, United States
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Sadzewicz, Lisa D.
, 
Mary Ann Jabra-Rizk

Mary Ann Jabra-Rizk

  • Department of Oncology and Diagnostic Sciences, School of Dentistry, University of MarylandBaltimore, United States
  • Department of Microbiology and Immunology, School of Medicine, University of MarylandBaltimore, United States
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Jabra-Rizk, Mary Ann
, 
Areej Alfaifi

Areej Alfaifi

  • Department of Oncology and Diagnostic Sciences, School of Dentistry, University of MarylandBaltimore, United States
  • Department of Restorative and Prosthetic Dental Sciences, College of Dentistry King Saud bin Abdulaziz University for Health SciencesRiyadh, Saudi Arabia
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Alfaifi, Areej
, 
Anmar Kensara

Anmar Kensara

  • Department of Advanced Oral Sciences and Therapeutics, School of Dentistry, University of MarylandBaltimore, United States
  • Department of Restorative Dentistry, College of Dentistry, Umm Al Qura UniversityMakkah, Saudi Arabia
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Kensara, Anmar
, 
Jason K. Molitoris

Jason K. Molitoris

  • University of Maryland Marlene and Stewart Greenebaum Comprehensive Cancer CenterBaltimore, United States
  • Department of Radiation Oncology, University of Maryland Medical CenterBaltimore, United States
  • Maryland Proton Treatment CenterBaltimore, United States
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Molitoris, Jason K.
, 
Matthew Witek

Matthew Witek

  • University of Maryland Marlene and Stewart Greenebaum Comprehensive Cancer CenterBaltimore, United States
  • Department of Radiation Oncology, University of Maryland Medical CenterBaltimore, United States
  • Maryland Proton Treatment CenterBaltimore, United States
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Witek, Matthew
, 
William S. Mendes

William S. Mendes

Department of Radiation Oncology, University of Maryland Medical CenterBaltimore, United States
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Mendes, William S.
, 
William F. Regine

William F. Regine

  • University of Maryland Marlene and Stewart Greenebaum Comprehensive Cancer CenterBaltimore, United States
  • Department of Radiation Oncology, University of Maryland Medical CenterBaltimore, United States
  • Maryland Proton Treatment CenterBaltimore, United States
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Regine, William F.
, 
Phuoc T. Tran

Phuoc T. Tran

  • Department of Radiation Oncology, University of Maryland Medical CenterBaltimore, United States
  • Maryland Proton Treatment CenterBaltimore, United States
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Tran, Phuoc T.
, 
Robert C. Miller

Robert C. Miller

Department of Radiation Medicine, University of Kentucky College of MedicineLexington, United States
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Miller, Robert C.
 und 
Ahmed S. Sultan

Ahmed S. Sultan

  • Department of Oncology and Diagnostic Sciences, School of Dentistry, University of MarylandBaltimore, United States
  • University of Maryland Marlene and Stewart Greenebaum Comprehensive Cancer CenterBaltimore, United States
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Sultan, Ahmed S.
  
23. Jan. 2024
A Longitudinal Metagenomic Comparative Analysis of Oral Microbiome Shifts in Patients Receiving Proton Radiation versus Photon Radiation for Head and Neck Cancer's Cover Image
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Artikel-Kategorie: Original Article
Online veröffentlicht: 23. Jan. 2024
Seitenbereich: 1 - 9
Eingereicht: 24. Aug. 2023
Akzeptiert: 01. Dez. 2023
DOI: https://doi.org/10.37029/jcas.v10i1.579
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© 2024 Timothy F. Meiller et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

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 characteristic IMRT (n=4) IMPT (n=4)
Mean age (range) 67 years (60–72) 62 years (54–77)
Male sex (percentage) 4 (100) 4 (100)
Caucasian race 3 (75) 4 (100)
Current cigarette smoking 3 (75) 2 (50)
Chemotherapy 2 (50) 2 (50)
Surgery 2 (50) 0 (0)
Histology 4 (100) SCC 4 (100) SCC
Tumor site 1 (25) Glossotonsillar1 (25) Base of tongue1 (25) Tonsil/Base of tongue1 (25) Supraglottic 1 (25) Glossotonsillar3 (75) Tonsil
HPV status 2 (50) Positive2 (50) Not performed 4 (100) Positive
Radiation parameters
Prescription dose 2 (50) 69.96 Gy2 (50) 60 Gy 4 (100) 69.96 Gy
Dose/fraction 2 (50) 2.12 Gy2 (50) 2 Gy 4 (100) 2.12 Gy
1 Fractions/day 4 (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)
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