A Narrative Review about Nutritional Management and Prevention of Oral Mucositis in Haematology and Oncology Cancer Patients Undergoing Antineoplastic Treatments
2. Materials and Methods
2.1. Literature Research
2.2. Study Eligibility, Selection, and Data Extraction
3.1. Summary of the Studies Included
3.1.1. Paediatric Population
3.1.4. Other Dietary Components or Prevention Methods
4.1. Paediatric Evidence
4.4. Vitamins and Amino Acids
4.5. Glycyrrhiza Glabra
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
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|Author (Year)||N||Study Design||Objective||Intervention||Time (Months)||Conclusions|
|Huang et al. (2019) ||59||RCT|
Phase III, double-blind
|To evaluate whether oral glutamine prevents acute toxicities (OM and dermatitis) secondary to the treatment with RT in patients with head and neck cancers.||Glutamine (TG);|
Control, maltodextrin (CG);
NCI CTCAE 4.03 version.
|19||CG developed more OM (grades 2–4) than TG; nevertheless, the efficacy of the treatment with oral glutamine was not meaningful after RT in head and neck cancers.|
|Tsujimoto et al. (2015) ||40||RCT, double-blind||To evaluate whether oral glutamine reduces mucositis severity induced by CRT in patients with head and neck cancer.||Glutamine (TG);|
NCI CTCAE 3.0 version.
|36||Oral glutamine reduced OM severity produced by CT in head and neck cancer patients with a maximum mean grade of OM lower for TG than for PG, a duration without meaningful difference between both groups, and a shorter duration of artificial nutrition required in TG.|
|Tanaka et al. (2016) ||30||RCT|
|To assess whether glutamine and the combination of glutamine and elemental diet reduce the incidence of CT induced OM in patients with oesophageal cancers.||Placebo (PG);|
Glutamine + elemental diet (CTG);
NCI CTCAE 3.0 version.
|36||No differences between PG and TG|
|Pachón-Ibañez et al. (2018) ||262||Prospective cohort study||To evaluate whether oral glutamine prevents mucositis induced by oncological therapies (CRT or RT) in patients with head and neck cancer.||Oral glutamine (TG);|
RTOG/EORTC (MO and oesophagitis).
|-||More OM in PG (RR:1.78), without remarkable differences in severity. Higher odynophagia in PG (RR:2.87), with more severity (R = 4.33). In PG, more discontinuity in the treatment.|
|Chang et al. (2019) ||60||RCT|
|To measure the impact of oral glutamine as a supplement for the prevention of oesophagitis induced by CRT in patients with advanced non-small cell lung cancer (stages III–IV).||Placebo (PG);|
Oral glutamine (TG);
ARIE, acute radiation induced oesophagitis.
|12||TG had less severe ARIE than PG, as well as a reduction in the incidence of weight loss in TG.|
|Anturlikar et al. (2019) ||20||In vitro and in vivo study||To measure the safety and efficacy of “HTOR-091516” (Tumeric, Triphala, and honey) as a treatment for OM induced by 5-FU (CT).||IN VITRO: gingival human fibroblast, mouse connective tissue, and human oral reconstructed epidermis culture. Later treatment with “HTOR-091516” and MTT test (cytotoxicity) + TNF-α inhibition test (inflammation)+ test INVITTOX |
SKINETHIC ™ (irritation).
IN VIVO: two groups of rats (control (PG) and treatment with “HTOR-091516” (TG)). In TG: drops on the induced ulcer in every animal during their treatment with CT.
|0.5 (14 days)||The average weight loss in TG was lower; there also was less mortality and a reduction in OM grade (WHO scale). The product is proposed to prevent OM.|
|Cho et al. (2019) ||91||CT||To assess the effect of glutamine-enriched parenteral nutrition (PN) on weight, infections, complications (mucositis, neutropenia, and graft-versus-host disease), and mortality in patients who underwent HSCT transplantation.||Control (CG);|
Glutamine (TG) through Dipeptiven© (bottle).
|48||No significant association in the case of OM duration. A reduction in 100-days mortality for TG was noted.|
|Shumsky et al. (2019) ||15||Pilot RCT||To evaluate the efficacy of Oncoxin (ONCX) in oncologic patients with OM who underwent CT, RT or both.||Control group (CG);|
Group ONCX (OG);
|0.6 (20 days)||Lower-grade OM was found in OG (after 7 days of treatment and towards the end of their treatment).|
|Widjaja et al. (2020) ||48||Double-blind RCT||To measure whether oral glutamine prevents OM during CT (methotrexate (MTX) in paediatric patients with acute lymphoblastic leukaemia (ALL).||Placebo group (PG);|
Oral glutamine group (TG);
|0.5 (14 days)||There was a reduction in the incidence and severity of OM in TG after CT.|
|Harada et al. (2018) ||50||In vitro and in vivo study||To appraise the efficacy of Elental© (dietetic liquid formulation enriched with amino acids, which is a source of L-glutamine) in 5-FU (CT)-induced OM and dermatitis treatment.||In vivo:|
Saline solution (PG);
Dextrin group (DG);
Elental group (EG).
|0.25 (8 days)||In vivo, OM healed faster than in EG.|
|Oosterom et al.|
|99 (A) and 81 (B)||Cohort study||(1) To study the prevalence of vitamin D deficiency in paediatric patients;|
(2) To establish a link between vitamin D levels and methotrexate (MTX)-induced OM in paediatric acute lymphoblastic leukaemia (ALL).
|Vitamin D levels before and after MTX therapy.|
After MTX, classification in two groups depending on OM grade: ≥3 or ≤3.
NCI CTCAE 3.0 version.
|2004–2012||There was no association between basal vitamin D levels and MTX-induced OM, but low levels of vitamin D during MTX therapy were found to be related to severe OM.|
|Sun et al. (2019)|
|100||Double-blind RCT||To examine the effects of a group B multivitamin complex combined with GeneTime© (human recombinant growth factor) on the treatment of OM in patients with head and neck cancer undergoing RT.||Control group with vitamin B complex.Observational group with (OG) vitamin B complex + GeneTime©.|
|12||Less severity, affected area, and healing time of the OM ulcers in OG.|
|Nejatinamini et al. (2018) |
|To evaluate the changes in vitamin status during the treatment of head and neck cancers related to body composition, inflammation, and mucositis.||Dietetic intake measurement (3 days).|
Vitamin levels (vitamins D, E, B9, and B12)
basal (before treatment) and 6 to 8 weeks after RT treatment (with or without CT); C-reactive protein (CRP) measurement.
C-reactive protein (CRP) baseline before and after 6 to 8 weeks of RT treatment, either with or without QT after treatment.
|1–1.5||Higher rates of OM were observed related to less vitamin D, B12, E, and B9 intake and lower blood levels of vitamin A and D.|
|Tanaka et al. (2018) ||19||RCT||To measure the intake of Elental© during two cycles of CT and to determine the incidence of OM in patients with oesophageal cancers treated with CT who completed their intake and those who did not completed it.||Elental© group (CG);|
Elental© group with uncompleted treatment (UG);
CTCAE 3.0 version.
|2 (56 days)||Less severity of OM in CG during CT with the use of Elental©.|
|Pathak et al. (2019) ||56||RCT||To assess the efficacy and role of oral glutamine in the treatment of OM and dysphagia induced by chemoradiotherapy (CRT) in patients with oropharynx and larynx carcinoma.||Control group (CG);|
Glutamine group (TG);
NCI CTCAE 4.03 version.
|1.75 (49 days)||TG had fewer hospitalizations due to OM and dysphagia.|
More incidence and severity of OM in CG.
|Mamgain et al. (2020) ||127||RCT||To evaluate the efficacy of an ayurvedic preparation (based on Glycyrrhiza glabra) in order to decrease the severity of mucositis in patients with head and neck cancers who received chemoradiotherapy (CRT).||Comparison between basal and post-RT characteristics:|
(1) Conventional OM treatment (antiacids and anaesthetics) (CTG);
(2) Conventional treatment and ayurvedic preparation (ATG);
(3) Honey and conventional treatment (HTG).
|24||Less severity, less pain, and shorter onset time of mucositis, both in ATG and HTG, but especially in ATG.|
|Harada et al. (2019) ||50||Open RCT||To evaluate changes in OM (injuries’ size, pain, and redness + CRP in plasma) in patients with oral squamous cell carcinoma undergoing CRT or RT with Elental© administration.||Elental group (EG);|
Non-Elental group as the control (CG);
CTCAE 4.0 version.
|24||In EG, milder OM development in CRT; no difference in RT.|
|Rao et al. (2017) ||49||Blinded single-centre RCT||To evaluate whether honey causes interference with RT-induced tumoral response or whether it exhibits a positive effect against OM in patients with head and neck cancer.||Povidone–iodine group (CG);|
Honey group (HG);
|6||Lower incidence of OM and less severity in HG. The implications for treatment interruption were not significant.|
|Branda et al. (2004) ||68||Pilot cohort study||To study the influence of B12 vitamin, folate, and dietetic supplements on CT-induced toxicity in breast cancer patients.||Blood samples (B12, B9, and neutrophils) before/after the first CT cycle;|
Questionnaires about supplement usage;
OM grading (author-modified CTCAE);
68 subjects + historical controls.
|-||No evidence of influence was found.|
|Okada et al. (2017) ||20||Pilot single-centre RCT||To evaluate the influence of Elental© on CT-induced OM and diarrhoeas in patients with oesophageal cancer.||IG: use of |
CG: no Elental used;
Questionnaires and clinical examination;
CTCAE 4.0 version.
|0.5 (14 days)||Less severe OM incidence in IG.|
|De Sousa et al. (2018) ||40||In vivo study||To evaluate the effects of glycine in the expression of collagen and platelet and epidermal growth factors (PDGF, EGF) in an OM murine model.||Control group (CG);|
Intervention group (IG: glycine supplementation);
Measurement of collagen percentage and type and EGF and PDGF percentage.
|-||Positive effects in IG, with a better recovering rate (collagen increase and growth factors reduction).|
|Nihei et al. (2018) ||67||Single-centre|
|To evaluate the efficacy and safety of L-Glutamine sodium azulene sulphonate in the treatment of CT-induced OM in patients with colorectal and breast cancer.||Intervention group (IG);|
Control group (CG: standard oral hygiene);
CTCAE 4.0 version;
NRS pain scale.
|24||Lesser OM severity in IG. No significant differences were found regarding incidence.|
|Chattopadhyay et al. (2014) ||70||Single-centre RCT||To evaluate the influence of oral glutamine on RT-induced OM in patients with head and neck cancer.||Intervention group with oral glutamine (IG);|
No placebo control group (CG);
|8||Lower incidence, severity, and duration of RT-induced OM in IG.|
|Üçüncü et al. (2006) ||35||Laboratory CT|
|To determine the preventive effect of Vitamin E (VE) and L-Carnitine (LC), alone or in combination, on OM and myelosuppression by RT.||5 groups:|
(1) No RT (control: saline + simulated radiation);
(3) RT + VE;
(4) RT + LC;
(5) RT + VE + LC.
OM measurement scale: Parkins et al.;
Clinical/histopathological OM was evaluated; Levels of SOD and CAT (antioxidants) and MDA (oxidative stress indicator).
4 days pre-RT—10 days post-RT.
|VE and LC proved to be radioprotective agents on their own and not combined together, with lower severity and longer time to histological appearance of OM.|
Good tolerance and no adverse effects.
|Amanat et al. (2017) ||82||Single-centre RCT||To assess the effect of honey on clinical grades of OM.||Honey group (HG);|
Control saline group (CG);
|12||Lower incidence and severity of OM in HG during the RT.|
|Podlesko et al. (2018) ||3||Case series||To evaluate the effects of topical application of deoxyribonucleic acid on three OM (moderate–severe) cases in patients with head and neck cancer.||Oral spray of polydeoxyribonucleotide (PDRN) as treatment.||1||Increased relief and remission of OM over time, without interruption in treatment or opioid intake.|
|Perrone et al. (2017) ||73||CT||To analyse the influence of dietary supplementation with whey protein concentrate (WPC) on the incidence of OM in patients undergoing HSCT.||WPC group (WG);|
Historical controls (CG);
WG was sub-stratified into: consumed <80% PWC (WG1) or ≥80% (WG2) of the offered dose;
WHO and CTCAE 4.0 version.
|Not specified||No significant differences between WG and CG in incidence, duration, and severity of OM concerns. However, in WG2, shorter duration and lower incidence of severe OM was found.|
|Ogata et al. (2017) ||22||Pilot prospective study||To evaluate the preventive effects of Elental ® on CT-induced OM in patients with colorectal cancer (CRC).||22 patients in Elental (1 group);|
CTCAE 3.0 version.
|36||Significantly reduced CT (5-FU)-induced OM grade.|
|Al Jouni et al. (2017) ||40||Open RCT||To evaluate the effects of honey on grade 3–4 OM, reduction in bacterial/fungal infections, duration of OM episodes, and body weight in paediatric leukaemia patients undergoing CT or RT.||Control group (CG) with Lidocaine, Mycostatin, Daktarin, and oral cleaning;|
Experimental group (HG) with same routine as CG + honey (4–6 times/day);
|12||Significant reduction in severity and pain in HG. Significant improvement in weight and time to OM onset in HG.|
|Lopez-Vaquero et al. (2017) ||49||Phase II double-blind RCT||To evaluate whether glutamine is effective in reducing the incidence and severity of mucositis and dermatitis induced by RT or CRT in patients with head and neck cancer.||L-Glutamine group (TG);|
Placebo group with malto-dextrine (PG);
CTCAE 3.0 version.
|6||Incidence and severity with no significant differences between groups.|
|Howlader et al. (2019) ||40||RCT (single-blinded).||To assess whether honey improves mucositis injuries and the quality of life of patients with RT/CT-induced OM (for head and neck cancer).||Treatment group (HG) with honey (both rinsed and ingested honey);|
Control group (CG) with saline solution;
|From CT start—4 weeks after RT.||Less OM and associated symptoms induced by RT in HG. Shorter time towards the recovery of a regular quality of life.|
|Elsass (2017) ||10|
|Case series||The aim was to improve OM (oral comfort and feeding) with standard oral care and the use of Leptospermum honey in paediatric oncology patients after proven CT.||Application of honey on the buccal surface with a cotton swab, 3 times/day, Then spat or suctioned out.||-||Shorter healing time with lower pain rate in all cases.|
|Elkerm and Tawashi (2014) |
|20||Pilot study||To evaluate whether date palm pollen (DPP) can be effective in the prevention and treatment of RT- and CT-induced OM in patients with head and neck cancer.||DPP group (one daily suspension);|
Control group (CG) (antifungal, rebamipide, and oral analgesia);
OMAS score and visual analogue scale for mouth pain and dysphagia.
|1.5 (6 weeks)||Significant reduction in incidence, severity, and pain in OM and dysphagia in DPP.|
|Raeessi et al. (2014) ||61||Single-centre double-blind RCT||To evaluate the effects of coffee + honey in the treatment of OM by CT and compare them with the effects of steroids.||3 groups:|
(1) Betamethasone group (EG);
(2) Honey group (HG);
(3) Honey + coffee group (HCG);
|Significant reduction in the severity of OM in all three groups.|
|Baydar et al. (2005) ||99||CT||To research the effects of local cryotherapy on the prevention of CT (5-FU)-induced OM.||Intervention group (IG): CT courses with local cryotherapy (ice in the mouth during the CT course up to 10 min afterwards);|
Control group (CG): no-cryotherapy courses.
|Not specified.||5-FU-induced OM incidence lower in GI (OR = 11.5).|
|Peterson et al. (2007) ||305||Phase III, double-blind RCT||To observe the efficacy of Saforis ® in the prevention and treatment of OM caused by CT treatment in breast cancer.||Saforis group (SG);|
Placebo group (PG) (with subsequent cross-linking);
WHO scale (ulcer grading scale); OMAS scale (ulceration measurement).
|Not specified.||Lower severity and incidence rate in SG.|
|Fogh et al. (2016) ||119||Multicentric phase II RCT||To evaluate the effect of Manuka honey (liquid and tablets) in the prevention of RT-induced oesophagitis in lung cancer patients.||G1: Manuka honey (liquid);|
G2: Manuka honey (tablets);
G3: control, standard care.
Measurements: odynophagia (NRPS scale), pain, opioid use, dysphagia, weight loss, quality of life, and nutritional status.
|12||There were no significant differences for groups G1, G2, or G3, so the use of honey did not prove to be superior to standard health care.|
|Samdariya et al. (2015) ||69||Open RCT||To study the intake of honey in pain relief caused by RT-induced OM in patients with head and neck cancer.||(1) Gargle with soda and benzidamine (PG);|
(2) Gargle with soda + benzidamine + honey (HG).
|November 2011–January 2013.||Slightly greater relief in HG during the entire follow-up (3 months), with a significant reduction in the severity of OM-associated pain and fewer treatment interruptions.|
|Matsuda et al. (2015) ||90||Double-blind phase III RCT.||To research whether TJ-14 (Hangeshashinto) prevents and/or controls CT-induced OM in patients with colorectal cancer.||TJ-14 treatment group (IG);|
Placebo group (PG);
|0.5 (14 days).||Significant reduction in the duration of severe OM, with no effect on the severity or incidence of OM itself.|
|Bateman et al. (2013) ||Not specified (approximate number = 48).||Laboratory in vivo study||To investigate the protective effects of nutritional drinks on the development of methotrexate (MTX)-induced gastrointestinal mucositis in animals with and without cancer.||G1: ClinutrenProtect ® (whey protein, short-chain fatty acids, TGF-b, L-glutamine);|
G2: IMPACT AdvancedRecovery ® (whey protein, medium chain fatty acids, arginine, nucleotides, and polyunsaturated fatty acids);
G3: placebo (drink);
Control: standard rat diet.
|Not specified.||Administered diets offered no observed protection against MTX-induced mucositis.|
|Jayachandran and Balaji (2012) ||60||RCT||To evaluate the effect of natural honey and benzidamine hydrochloride on the development and severity of RT-associated OM in patients with oral cancers.||3 groups (oral rinses):|
(1) Honey (HG);
(2) Benzidamine hydrochloride (BG);
(3) Saline 0.9% (control group, CG).
|6||Lower severity and earlier healing of OM not significant in HG.|
|Sugita et al. (2012) ||118||Retrospective CT||To ascertain the effects of folinic acid administration (systemic and rinsed) on the incidence of OM and acute graft-versus-host disease (GVHD) after GVHD prophylaxis with MTX in patients undergoing HSCT.||Systemic folic acid was administered to patients at increased risk of developing OM (n = 29).||48||Folinic acid could be useful in reducing the incidence of severe OM, both in systemic use and rinsed.|
|Sorensen et al. (2008) ||206||Double-blind RCT||To evaluate prevention of OM using chlorhexidine compared with cryotherapy during 5-FU CT in gastrointestinal cancer.||3 groups:|
(1) Chlorhexidine rinse (IG);
(2) Placebo rinse (saline) (PG);
(3) Cryotherapy (CG).
|-||Higher severity rate of OM in PG and lower in CG, with a lower incidence and duration in IG and CG than in PG; therefore, prophylaxis seems effective in both IG and CG.|
|Das et al. (2011) ||52||RCT||Observe protective/healing effect against RT and CT effects (OM, skin reaction, xerostomia, or voice changes) when using Glycyrrhiza glabra.||4 groups:|
(1) Glycyrrhiza + local honey and oral Glycyrrhiza (GLHG);
(2) Glycyrrhiza + local honey (LHG);
(3) Topical honey (HG);
(4) Control (conventional modern medication) (CG).
|1.75 (7 weeks)||Lower incidence and severity in GLHG and LHG compared with CG, but similar to HG.|
|Thornley et al. (2004) ||37||CT||To determine the feasibility and potential efficacy of a fixed combination of agents in reducing RRT (regimen-related toxicity) in children undergoing HSCT.||Combination group of ursodeoxycholic acid (UDCA), vitamin E, folinic acid, and titrated parenteral nutrition (IG);|
Historical control group (1995–2000) (PG).
|36||Significant decrease in the incidence and severity of OM in IG.|
|Iyama et al. (2014) ||44||RCT||To research whether supplementation with GFO (glutamine, fibre, oligosaccharides) decreases the severity of mucosal injury post-HSCT.||GFO group (IG);|
CTCAE 4.0 version.
|36||Significant decrease in OM and higher survival rate in IG.|
|Takano et al. (2015) |
|96-well plates||In vitro study||To investigate whether γ-tocotrienol (vitamin E) can enhance survival of oral human keratinocytes (RT7) against 5-FU-induced cell toxicity.||RT7 cells were treated with 5-FU and γ-tocotrienol.|
(3) γ-tocotrienol + 5-FU;
(4) Control de 5-FU + N-acetylcysteine.
|-||In C there was a significant inhibition of ROS production induced by 5-FU.|
|Agha-Hosseini et al. (2021) |
|59||Triple-blind RCT||To evaluate whether a vitamin E, hyaluronic acid, and triamcinolone mouthwash was effective in the treatment of radiotherapy-induced OM grades 3–4.||Group with vitamin E + hyaluronic acid + triamcinolone rinses (IG);|
Group with triamcinolone rinses (CG).
|4 weeks||Significant reduction in the severity of RT-induced OM in IG over time.|
|Yeshurun et al. (2020) ||52||Multicentre double blind RCT||To determine whether folinic acid (FA) reduces methotrexate (MTX)-induced toxicity in patients undergoing myeloablative conditioning (CM) for allogeneic haematopoietic cell transplantation, who have also received MTX prophylaxis for graft-versus-host disease.||TG with FA;|
PG with placebo;
|17 (4.5–50)||There were no significant TG and PG differences in incidence, duration, or severity of OM.|
|Pattanakitsakul et al. (2020) |
|30||Preliminary and single-centre quasi-randomized trial||To examine the protective effect of vitamin A supplementation against mucosal damage of the gastrointestinal tract after CT in paediatric patients undergoing HSCT. As a secondary objective, to assess the occurrence of OM.||TG with single dose (200000 IU) of vitamin A;|
PG without vitamin A;
|12||There were no significant differences in incidence or severity of OM.|
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García-Gozalbo, B.; Cabañas-Alite, L. A Narrative Review about Nutritional Management and Prevention of Oral Mucositis in Haematology and Oncology Cancer Patients Undergoing Antineoplastic Treatments. Nutrients 2021, 13, 4075. https://doi.org/10.3390/nu13114075
García-Gozalbo B, Cabañas-Alite L. A Narrative Review about Nutritional Management and Prevention of Oral Mucositis in Haematology and Oncology Cancer Patients Undergoing Antineoplastic Treatments. Nutrients. 2021; 13(11):4075. https://doi.org/10.3390/nu13114075Chicago/Turabian Style
García-Gozalbo, Balma, and Luis Cabañas-Alite. 2021. "A Narrative Review about Nutritional Management and Prevention of Oral Mucositis in Haematology and Oncology Cancer Patients Undergoing Antineoplastic Treatments" Nutrients 13, no. 11: 4075. https://doi.org/10.3390/nu13114075