Skip to main content
Top
Published in:

Open Access 01-12-2024 | Radiotherapy | Research

Effect of blood oxidative stress indicators on oral mucositis in patients undergoing radiotherapy for nasopharyngeal carcinoma

Authors: HongXia Pang, SuZhen Li, XiaoYi Fu, ShaoMin Wen, DanYu Chen, XiaoChun Sun, Yong Chen, Song Yang

Published in: European Journal of Medical Research | Issue 1/2024

Login to get access

Abstract

Objectives

To investigate the correlation of total antioxidant capacity (T-AOC), glutathione peroxidase (GSH-PX), and advanced oxidized protein product (AOPP) levels in the progression of oral mucositis (OM) during nasopharyngeal carcinoma (NPC) radiotherapy.

Methods

This prospective study included 102 patients diagnosed with NPC and eligible for radiotherapy indications. T-AOC, GSH-PX, and AOPP were measured before treatment (T0) and during the second week (T1), fourth week (T2), and sixth week (T3) of the intensity-modulated radiation therapy (IMRT) period. Patients were categorized into severe OM (SOM) (n = 21) and Non-SOM (n = 81) groups at week 6. Serum T-AOC, GSH-PX, and AOPP levels were compared at different time periods. The trends of these markers in the two groups during the course of treatment were analyzed. Finally, stepwise logistic regression was conducted to analyze the risk factors for SOM in NPC patients undergoing IMRT.

Results

At T1 and T2 of IMRT, T-AOC and GSH-PX were higher in the SOM group than in the Non-SOM group; At T3, T-AOC and GSH-PX were lower in the SOM group than in the Non-SOM group. T-AOC and GSH-PX had similar change trends in Non-SOM or SOM patients, i.e., T-AOC levels continued to increase at T2 and decreased at T3, and GSH-PX increased significantly at T2 and decreased at T3. Of interest was the fact that T-AOC and GSH-PX decreased significantly more in SOM patients than in Non-SOM patients at T3, and that AOPP levels were in a constant state of increase in SOM patients. Preoperative hypoproteinemia, the absence of oral mucosal protective agents, and the receipt of synchronous chemotherapy were independent risk factors for increasing the course of OM in patients with NPC.

Conclusions

NPC patients undergoing IMRT exhibit dynamic alterations in blood T-AOC, GSH-PX, and AOPP. Notably, the persistent elevation of these biomarkers, particularly AOPP, is significantly associated with the progression of SOM in these patients. These findings underscore the involvement of oxidative stress imbalance in the pathogenesis of oral mucositis following IMRT.
Literature
2.
go back to reference Yang Q, Nie YH, Cai MB, Li ZM, Zhu HB, Tan YR. Gemcitabine combined with cisplatin has a better effect in the treatment of recurrent/metastatic advanced nasopharyngeal carcinoma. Drug Des Dev Ther. 2022;16:1191–8.CrossRef Yang Q, Nie YH, Cai MB, Li ZM, Zhu HB, Tan YR. Gemcitabine combined with cisplatin has a better effect in the treatment of recurrent/metastatic advanced nasopharyngeal carcinoma. Drug Des Dev Ther. 2022;16:1191–8.CrossRef
3.
go back to reference Su SF, Han F, Zhao C, Chen CY, Xiao WW, Li JX, et al. Long-term outcomes of early-stage nasopharyngeal carcinoma patients treated with intensity-modulated radiotherapy alone. Int J Radiat Oncol Biol Phys. 2012;82(1):327–33.CrossRefPubMed Su SF, Han F, Zhao C, Chen CY, Xiao WW, Li JX, et al. Long-term outcomes of early-stage nasopharyngeal carcinoma patients treated with intensity-modulated radiotherapy alone. Int J Radiat Oncol Biol Phys. 2012;82(1):327–33.CrossRefPubMed
5.
go back to reference Vesty A, Gear K, Biswas K, Mackenzie BW, Taylor MW, Douglas RG. Oral microbial influences on oral mucositis during radiotherapy treatment of head and neck cancer. Support Care Cancer. 2020;28(6):2683–91.CrossRefPubMed Vesty A, Gear K, Biswas K, Mackenzie BW, Taylor MW, Douglas RG. Oral microbial influences on oral mucositis during radiotherapy treatment of head and neck cancer. Support Care Cancer. 2020;28(6):2683–91.CrossRefPubMed
6.
go back to reference Feller L, Essop R, Wood NH, Khammissa RA, Chikte UM, Meyerov R, et al. Chemotherapy- and radiotherapy-induced oral mucositis: pathobiology, epidemiology and management. SADJ. 2010;65(8):372–4.PubMed Feller L, Essop R, Wood NH, Khammissa RA, Chikte UM, Meyerov R, et al. Chemotherapy- and radiotherapy-induced oral mucositis: pathobiology, epidemiology and management. SADJ. 2010;65(8):372–4.PubMed
7.
go back to reference Villa A, Vollemans M, De Moraes A, Sonis S. Concordance of the WHO, RTOG, and CTCAE v4.0 grading scales for the evaluation of oral mucositis associated with chemoradiation therapy for the treatment of oral and oropharyngeal cancers. Support Care Cancer. 2021;29(10):6061–8.CrossRefPubMed Villa A, Vollemans M, De Moraes A, Sonis S. Concordance of the WHO, RTOG, and CTCAE v4.0 grading scales for the evaluation of oral mucositis associated with chemoradiation therapy for the treatment of oral and oropharyngeal cancers. Support Care Cancer. 2021;29(10):6061–8.CrossRefPubMed
8.
go back to reference Ito K, Tokura S, Takazawa I, Yoshida N, Nakanishi T, Akiyama K, et al. Clinical investigation of use of Episil® oral solution in oral mucositis during radiotherapy for head and neck cancer. Heliyon. 2023;9(6): e15869.CrossRefPubMedPubMedCentral Ito K, Tokura S, Takazawa I, Yoshida N, Nakanishi T, Akiyama K, et al. Clinical investigation of use of Episil® oral solution in oral mucositis during radiotherapy for head and neck cancer. Heliyon. 2023;9(6): e15869.CrossRefPubMedPubMedCentral
9.
go back to reference Münstedt K. Topical application of honey in the management of chemo/radiotherapy-induced oral mucositis: comment on Yang et al. 2019. Int J Nurs Stud. 2019;92:57.CrossRefPubMed Münstedt K. Topical application of honey in the management of chemo/radiotherapy-induced oral mucositis: comment on Yang et al. 2019. Int J Nurs Stud. 2019;92:57.CrossRefPubMed
10.
go back to reference Bergamaschi L, Vincini MG, Zaffaroni M, Pepa M, Angelicone I, Astone A, et al. Management of radiation-induced oral mucositis in head and neck cancer patients: a real-life survey among 25 Italian radiation oncology centers. Support Care Cancer. 2023;32(1):38.CrossRefPubMedPubMedCentral Bergamaschi L, Vincini MG, Zaffaroni M, Pepa M, Angelicone I, Astone A, et al. Management of radiation-induced oral mucositis in head and neck cancer patients: a real-life survey among 25 Italian radiation oncology centers. Support Care Cancer. 2023;32(1):38.CrossRefPubMedPubMedCentral
11.
go back to reference Chaouni S, Lecomte DD, Stefan D, Leduc A, Barraux V, Leconte A, et al. The possibility of using genotoxicity, oxidative stress and inflammation blood biomarkers to predict the occurrence of late cutaneous side effects after radiotherapy. Antioxidants. 2020;9(3):220.CrossRefPubMedPubMedCentral Chaouni S, Lecomte DD, Stefan D, Leduc A, Barraux V, Leconte A, et al. The possibility of using genotoxicity, oxidative stress and inflammation blood biomarkers to predict the occurrence of late cutaneous side effects after radiotherapy. Antioxidants. 2020;9(3):220.CrossRefPubMedPubMedCentral
12.
go back to reference Jiang Y, Zhao D, Sun J, Luo X, Li H, Sun X, et al. Analysis of antioxidant effect of two tripeptides isolated from fermented grains (Jiupei) and the antioxidative interaction with 4-methylguaiacol, 4-ethylguaiacol, and vanillin. Food Sci Nutr. 2019;7(7):2391–403.CrossRefPubMedPubMedCentral Jiang Y, Zhao D, Sun J, Luo X, Li H, Sun X, et al. Analysis of antioxidant effect of two tripeptides isolated from fermented grains (Jiupei) and the antioxidative interaction with 4-methylguaiacol, 4-ethylguaiacol, and vanillin. Food Sci Nutr. 2019;7(7):2391–403.CrossRefPubMedPubMedCentral
13.
go back to reference Cirillo N, Vicidomini A, McCullough M, Gambardella A, Hassona Y, Prime SS, et al. A hyaluronic acid-based compound inhibits fibroblast senescence induced by oxidative stress in vitro and prevents oral mucositis in vivo. J Cell Physiol. 2015;230(7):1421–9.CrossRefPubMed Cirillo N, Vicidomini A, McCullough M, Gambardella A, Hassona Y, Prime SS, et al. A hyaluronic acid-based compound inhibits fibroblast senescence induced by oxidative stress in vitro and prevents oral mucositis in vivo. J Cell Physiol. 2015;230(7):1421–9.CrossRefPubMed
14.
go back to reference Zhu XX, Yang XJ, Chao YL, Zheng HM, Sheng HF, Liu HY, et al. The potential effect of oral microbiota in the prediction of mucositis during radiotherapy for nasopharyngeal carcinoma. EBioMedicine. 2017;18:23–31.CrossRefPubMedPubMedCentral Zhu XX, Yang XJ, Chao YL, Zheng HM, Sheng HF, Liu HY, et al. The potential effect of oral microbiota in the prediction of mucositis during radiotherapy for nasopharyngeal carcinoma. EBioMedicine. 2017;18:23–31.CrossRefPubMedPubMedCentral
15.
go back to reference Tan BL, Norhaizan ME, Liew WP, Sulaiman RH. Antioxidant and oxidative stress: a mutual interplay in age-related diseases. Front Pharmacol. 2018;9:1162.CrossRefPubMedPubMedCentral Tan BL, Norhaizan ME, Liew WP, Sulaiman RH. Antioxidant and oxidative stress: a mutual interplay in age-related diseases. Front Pharmacol. 2018;9:1162.CrossRefPubMedPubMedCentral
16.
go back to reference Bagyura Z, Takács A, Kiss L, Dósa E, Vadas R, Nguyen TD, et al. Level of advanced oxidation protein products is associated with subclinical atherosclerosis. BMC Cardiovasc Disord. 2022;22(1):5.CrossRefPubMedPubMedCentral Bagyura Z, Takács A, Kiss L, Dósa E, Vadas R, Nguyen TD, et al. Level of advanced oxidation protein products is associated with subclinical atherosclerosis. BMC Cardiovasc Disord. 2022;22(1):5.CrossRefPubMedPubMedCentral
17.
go back to reference Xiao B, Li D, Liao B, Zheng H, Yang X, Xie Y, et al. Effects of microplastics exposure on the Acropora sp. antioxidant, immunization and energy metabolism enzyme activities. Front Microbiol. 2021;12: 666100.CrossRefPubMedPubMedCentral Xiao B, Li D, Liao B, Zheng H, Yang X, Xie Y, et al. Effects of microplastics exposure on the Acropora sp. antioxidant, immunization and energy metabolism enzyme activities. Front Microbiol. 2021;12: 666100.CrossRefPubMedPubMedCentral
18.
go back to reference Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, et al. Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int. 2014;2014: 761264.CrossRefPubMedPubMedCentral Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, et al. Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int. 2014;2014: 761264.CrossRefPubMedPubMedCentral
19.
go back to reference Tang LL, Chen YP, Chen CB, Chen MY, Chen NY, Chen XZ, et al. The Chinese Society of Clinical Oncology (CSCO) clinical guidelines for the diagnosis and treatment of nasopharyngeal carcinoma. Cancer Commun. 2021;41(11):1195–227.CrossRef Tang LL, Chen YP, Chen CB, Chen MY, Chen NY, Chen XZ, et al. The Chinese Society of Clinical Oncology (CSCO) clinical guidelines for the diagnosis and treatment of nasopharyngeal carcinoma. Cancer Commun. 2021;41(11):1195–227.CrossRef
20.
go back to reference Rodríguez-Caballero A, Torres-Lagares D, Robles-García M, Pachón-Ibáñez J, González-Padilla D, Gutiérrez-Pérez JL. Cancer treatment-induced oral mucositis: a critical review. Int J Oral Maxillofac Surg. 2012;41(2):225–38.CrossRefPubMed Rodríguez-Caballero A, Torres-Lagares D, Robles-García M, Pachón-Ibáñez J, González-Padilla D, Gutiérrez-Pérez JL. Cancer treatment-induced oral mucositis: a critical review. Int J Oral Maxillofac Surg. 2012;41(2):225–38.CrossRefPubMed
21.
go back to reference Wu F, Wang R, Lu H, Wei B, Feng G, Li G, et al. Concurrent chemoradiotherapy in locoregionally advanced nasopharyngeal carcinoma: treatment outcomes of a prospective, multicentric clinical study. Radiother Oncol. 2014;112(1):106–11.CrossRefPubMed Wu F, Wang R, Lu H, Wei B, Feng G, Li G, et al. Concurrent chemoradiotherapy in locoregionally advanced nasopharyngeal carcinoma: treatment outcomes of a prospective, multicentric clinical study. Radiother Oncol. 2014;112(1):106–11.CrossRefPubMed
22.
go back to reference Al-Ansari S, Zecha JA, Barasch A, de Lange J, Rozema FR, Raber-Durlacher JE. Oral mucositis induced by anticancer therapies. Curr Oral Health Rep. 2015;2(4):202–11.CrossRefPubMedPubMedCentral Al-Ansari S, Zecha JA, Barasch A, de Lange J, Rozema FR, Raber-Durlacher JE. Oral mucositis induced by anticancer therapies. Curr Oral Health Rep. 2015;2(4):202–11.CrossRefPubMedPubMedCentral
24.
go back to reference Derindağ G, Akgül HM, Kızıltunç A, Özkan H, Kızıltunç Özmen H, Akgül N. Evaluation of saliva glutathione, glutathione peroxidase, and malondialdehyde levels in head-neck radiotherapy patients. Turk J Med Sci. 2021;51(2):644–9.CrossRefPubMedPubMedCentral Derindağ G, Akgül HM, Kızıltunç A, Özkan H, Kızıltunç Özmen H, Akgül N. Evaluation of saliva glutathione, glutathione peroxidase, and malondialdehyde levels in head-neck radiotherapy patients. Turk J Med Sci. 2021;51(2):644–9.CrossRefPubMedPubMedCentral
25.
go back to reference Alagozlu H, Gorgul A, Bilgihan A, Tuncer C, Unal S. Increased plasma levels of advanced oxidation protein products (AOPP) as a marker for oxidative stress in patients with active ulcerative colitis. Clin Res Hepatol Gastroenterol. 2013;37(1):80–5.CrossRefPubMed Alagozlu H, Gorgul A, Bilgihan A, Tuncer C, Unal S. Increased plasma levels of advanced oxidation protein products (AOPP) as a marker for oxidative stress in patients with active ulcerative colitis. Clin Res Hepatol Gastroenterol. 2013;37(1):80–5.CrossRefPubMed
26.
go back to reference Ozenirler S, Erkan G, Konca Degertekin C, Ercin U, Cengiz M, Bilgihan A, et al. The relationship between advanced oxidation protein products (AOPP) and biochemical and histopathological findings in patients with nonalcoholic steatohepatitis. J Dig Dis. 2014;15(3):131–6.CrossRefPubMed Ozenirler S, Erkan G, Konca Degertekin C, Ercin U, Cengiz M, Bilgihan A, et al. The relationship between advanced oxidation protein products (AOPP) and biochemical and histopathological findings in patients with nonalcoholic steatohepatitis. J Dig Dis. 2014;15(3):131–6.CrossRefPubMed
27.
go back to reference Li M, Hassan FU, Tang Z, Peng L, Liang X, Li L, et al. Mulberry leaf flavonoids improve milk production, antioxidant, and metabolic status of water buffaloes. Front Vet Sci. 2020;7:599.CrossRefPubMedPubMedCentral Li M, Hassan FU, Tang Z, Peng L, Liang X, Li L, et al. Mulberry leaf flavonoids improve milk production, antioxidant, and metabolic status of water buffaloes. Front Vet Sci. 2020;7:599.CrossRefPubMedPubMedCentral
28.
go back to reference Kim CH, Kim MS, Kang MJ, Kim HH, Park NJ, Jung HK. Oral mucosa pressure ulcers in intensive care unit patients: a preliminary observational study of incidence and risk factors. J Tissue Viability. 2019;28(1):27–34.CrossRefPubMed Kim CH, Kim MS, Kang MJ, Kim HH, Park NJ, Jung HK. Oral mucosa pressure ulcers in intensive care unit patients: a preliminary observational study of incidence and risk factors. J Tissue Viability. 2019;28(1):27–34.CrossRefPubMed
29.
go back to reference Gobbo M, Joy J, Guedes H, Shazib MA, Anderson C, Abdalla-Aslan R, et al. Emerging pharmacotherapy trends in preventing and managing oral mucositis induced by chemoradiotherapy and targeted agents. Expert Opin Pharmacother. 2024;25(6):727–42.CrossRefPubMed Gobbo M, Joy J, Guedes H, Shazib MA, Anderson C, Abdalla-Aslan R, et al. Emerging pharmacotherapy trends in preventing and managing oral mucositis induced by chemoradiotherapy and targeted agents. Expert Opin Pharmacother. 2024;25(6):727–42.CrossRefPubMed
30.
go back to reference Minhas S, Sajjad A, Chaudhry RM, Zahid H, Shahid A, Kashif M. Assessment and prevalence of concomitant chemo-radiotherapy-induced oral mucositis in patients with oral squamous cell carcinoma. Turk J Med Sci. 2021;51(2):675–84.CrossRefPubMedPubMedCentral Minhas S, Sajjad A, Chaudhry RM, Zahid H, Shahid A, Kashif M. Assessment and prevalence of concomitant chemo-radiotherapy-induced oral mucositis in patients with oral squamous cell carcinoma. Turk J Med Sci. 2021;51(2):675–84.CrossRefPubMedPubMedCentral
31.
go back to reference Zhang Y, Chen L, Hu GQ, Zhang N, Zhu XD, Yang KY, et al. Final overall survival analysis of gemcitabine and cisplatin induction chemotherapy in nasopharyngeal carcinoma: a multicenter, randomized phase III trial. J Clin Oncol. 2022;40(22):2420–5.CrossRefPubMed Zhang Y, Chen L, Hu GQ, Zhang N, Zhu XD, Yang KY, et al. Final overall survival analysis of gemcitabine and cisplatin induction chemotherapy in nasopharyngeal carcinoma: a multicenter, randomized phase III trial. J Clin Oncol. 2022;40(22):2420–5.CrossRefPubMed
Metadata
Title
Effect of blood oxidative stress indicators on oral mucositis in patients undergoing radiotherapy for nasopharyngeal carcinoma
Authors
HongXia Pang
SuZhen Li
XiaoYi Fu
ShaoMin Wen
DanYu Chen
XiaoChun Sun
Yong Chen
Song Yang
Publication date
01-12-2024
Publisher
BioMed Central
Keyword
Radiotherapy
Published in
European Journal of Medical Research / Issue 1/2024
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-024-02137-3