Braz Dent J (2009) 20(3): 215-220 Laser and oral mucositis 215

ISSN 0103-6440

Use of Therapeutic Laser for Prevention

and Treatment of Oral Mucositis

Vivian Youssef KHOURI

Ana Beatriz Pereira Lima STRACIERI
Maria Carolina RODRIGUES
Daniela Aparecida de MORAES
Fabiano PIERONI
Belinda Pinto SIMÕES
Júlio César VOLTARELLI

University Hospital, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil

Oral mucositis (OM) affects patients who are submitted to hematopoietic stem cell transplantation (HSCT) due to high doses of che-
motherapy and/or radiotherapy. The purpose of this investigation was to perform a comparative study of the frequency and evolution
of OM among patients subjected to therapeutic laser and to the conventional therapy (use of mouthwash called “Mucositis Formula”).
The patients were subjected to a myeloablative conditioning regimen before the allogeneic HSCT. Twenty-two patients were selected
and divided into 2 groups: group I was irradiated with InGaAlP laser (660 nm) and GaAlAs laser (780 nm), 25 mW potency, 6.3J/
cm2 dose, in 10-s irradiation time, followed to conventional treatment; group II was subjected only to the conventional treatment.
Both World Health Organization (WHO) scale and the Oral Mucositis Assessment Scale (OMAS) were used to evaluate the results.
Data were analyzed by the non-parametric Wilcoxon test, with p<0.05 considered as statistically significant. Group I presented a
lower frequency of OM (p=0.02) and lower mean scores, according to WHO and OMAS scales (p<0.01 and p=0.01, respectively).
In conclusion, laser reduced the frequency and severity of OM, suggesting that therapeutic laser can be used both as a new form of
prevention and treatment of OM.

Key Words: oral mucositis, chemotherapy, radiotherapy, allogeneic hematopoietic stem cell transplantation, therapeutic laser.

INTRODUCTION the oropharynx. It mainly affects patients subjected to

aggressive myeloablative chemotherapy associated or
Hematopoietic stem cell transplantation (HSCT) not with radiotherapy, procedures that are also used in
or bone marrow transplantation is used as a thera- conditioning regimens for HCST (4,5). The incidence
peutic modality for malignant and non-malignant of mucositis in these patients is approximately 80 to
hematological diseases, severe immunodeficiences 100% (6). Clinically, mucositis starts in an asymptomatic
and bone marrow aplasia (1). HSCT requires the applica- manner, followed by the presence of erythema, burning
tion of a conditioning regimen leading to myeloablation in complaints and increased sensitivity to hot and spicy
order to create a space in the bone marrow of the recipient foods. The erythema may progress to areas of desqua-
(2). Immunosuppression and destruction of neoplastic mation, followed by the appearance of ulcers associated
cells are other effects of high doses of chemotherapeutic with dysphagia and reduced oral ingestion, with a series
drugs in combination or not with whole body radiotherapy. of clinical consequences that affect the quality of life
Oral mucositis (OM) is a common complication of the patients (6).
of cytotoxic chemotherapy and radiotherapy (3). This In view of the complexity of this toxicity, there
condition affects the mucosa of the gastrointestinal is no standard of prevention or treatment, with a di-
tract and especially the mucosa of the oral cavity and versified management of OM. In our Bone Marrow

Correspondence: Vivian Youssef Khouri, Unidade de Transplante de Medula Óssea do Hospital das Clínicas da Faculdade de Medicina de Ribeirão
Preto, USP, Avenida Bandeirantes, 3900, 14048-900 Ribeirão Preto, SP, Brasil. Tel: + 55-16-3602-2609. e-mail: [email protected]

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216 V.Y. Khouri et al.

Transplant Unit (BMTU) of the University Hospital of kg) with fludarabine (D-6 to D-2, 30 mg/m2), 4 patients
the School of Medicine of Ribeirão Preto, University received total body irradiation (D-6 to D-4, 990 cGy
of São Paulo (UHSMRP/USP), Brazil, a mouthwash total) and cyclophosphamide (D-3 to D-2, 60 mg/kg/)
known as “Mucositis Formula” has been used for the and 1 patient received fludarabine (30 mg/m2)/citarabine
treatment of clinical manifestations of OM, such as pain, (2000 mg/m2)/mitoxantrone (10 mg/m2) from D-10 to
erythema and ulceration. This oral rinse was developed D-7 and melfalan (D-3 to D-2, 70 mg/m2).
at the UHSMRP/USP, Brazil, and is a combination of All patients were subjected to treatment with
antiinflammatory (benzidamine), antifungal (nistatin) methotrexate in combination with cyclosporine after
and anesthetic agents (neututocain) and distilled water. transplantation for prevention of graft-versus-host
Rubenstein et al. (7) described experimental disease.
therapies using for the prevention or treatment of OM Inclusion criteria were: 12 years of age or older,
such as cryotherapy, benzidamine and palifermin, which both genders, hematologic or onco-hematologic disease,
reduced the severity of mucositis. According to Campos myeloablative conditioning regimen, and allogeneic
et al. (8), laser therapy offers as a new approach for the hematopoietic stem cell transplantation. Exclusion cri-
prevention and treatment of OM, reducing the pain and teria were: autoimmune disease, non-myeloablative
stimulating the salivary glands. conditioning regimen, and haploidentical or autologous
In view of the small number of studies on the hematopoietic stem cell transplantation. Groups I and II
use of therapeutic laser for the prevention and treat- were subjected to different protocols for the prevention
ment of OM, this study compared the frequency and and treatment of OM.
course of OM between groups of patients managed with The prevention phase for both groups started on
therapeutic laser and conventional treatment (“Mucositis the first day of conditioning and lasted until the initial
Formula”). clinical manifestation of mucositis in the oral cavity.
The standard protocol for oral hygiene consisted of
MATERIAL AND METHODS using soft-bristle toothbrushes and rinsing with 0.9%
saline 4 times a day after meals, followed by rinsing
The study was conducted at the BMTU of the with a benzidamine solution at the same frequency.
UHSMRP/USP, Ribeirão Preto, SP, Brazil, from March In the beginning of 2006, the benzidamine solution
2004 to September 2006, with the participation of 22 was replaced by an alcohol-free 0.12% chlorhexidine
patients subjected to allogeneic HSCT. The study was
approved by the local Research Ethics Committee
(Protocol #1534/2004) and all subjects gave written Table 1. Demographic and clinical characteristics of the patients.
informed consent to participate in the study.
The patients were randomized into 2 groups ac- Group I Group II
cording to the order of hospitalization. Demographic Laser therapy Mucositis Formula
(n=12) (n=10)
characteristics of both groups are shown in Table 1.
The conditioning regimen (high dose chemo-
Mean age (years) 32.7 27.5
therapy) was given to the 2 groups before stem cell infu-
sion. In group I, 2 patients received cyclophosphamide Gender
(D-5 to D-2, 50 mg/kg), 6 patients received busulfan Male 10 7
(D-7 to D-4, 1 mg/kg) with cyclophosphamide (D-3 Female 2 3
to D-2, 60 mg/kg), 3 patients received busulfan (D-6
Diagnosis
to D-3, 1 mg/kg) with fludarabine (D-6 to D-2, 30 mg/
m2) and 1 patient received total body irradiation (D-6 Acute myeloid leukemia 5 3
to D-4, 990 cGy total) and cyclophosphamide (D-3 to Acute lymphoid leukemia 1 2
D-2, 60 mg/kg).
Chronic myeloid leukemia 3 2
In group II, 1 patient received busulfan (D-7 to
D-4, 1 mg/kg) with cyclophosphamide (D-3 to D-2, 60 Severe aplastic anemia 2 2
mg/kg), 2 patients received busulfan (D-6 to D-3, 1 mg/ Myelodysplastic syndrome 1 1

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 Laser and oral mucositis 217

gluconate solution. improvement after laser, without persuade results. The

The treatment phase for both groups started with study was not blinded because group II was subjected
the initial clinical manifestations of mucositis (e.g.: only to the conventional treatment and not to sham laser.
pain, edema, erythema) with follow-up until D+15 after A low-intensity laser device (Twin Laser; MM
transplantation, and consisting of the combination of Optics Ltda., São Carlos, SP, Brazil) purchased by our
the standard oral hygiene protocol with the use of the BMTU in 2003 was used in this study. The present
“Mucositis Formula” mouthwash. The composition of study differed from the studies reported in the literature
this rinse is: 0.15 g benzidamine, 1.13 g nistatin, 2 g in that we compared the effect of laser therapy to that
neututocain and 10 mL distilled water. Benzidamine is of conventional therapy. Several irradiation parameters
an antiinflammatory agent that can reduce the production were studied in order to determine the most adequate
of pro-inflammatory cytokines and free radicals. Nistatin parameter settings to be used in the study. Two types
is a topical antifungal agent used for the treatment of of laser with the following diodes were used: indium
oral candidiasis, the main opportunistic infection related gallium aluminum phosphide (InGaAlP) with 660 nm
to OM, and neututocain (an anesthetic) is used for pain wavelength and gallium aluminum arsenide (GaAlAs)
relief. The difference between these 2 protocols was the with 780 nm wavelength. The first diode emits a visible
inclusion of laser therapy both during the prevention and red laser, has lower penetration into biological tissue
the treatment phase in group I. and is indicated for tissue repair, while the second diode
Two scales were used for evaluation of OM: emits infrared laser, has greater penetration capacity
World Health Organization (WHO) Oral Toxicity Scale and it is indicated for analgesia. The laser applications
and Oral Mucositis Assessment Scale (OMAS). In the were performed daily in the morning, once a day, and
WHO scale, WHO 0 is defined no abnormality, WHO 1 the 2 lasers were applied on alternate days using the
is erythema requiring no treatment, WHO 2 is presence same irradiation parameters: 25 mW output power, 10-s
of pain requiring no analgesics, difficulty in feeding, irradiation time and 6.3 J/cm2 dose per site and with
WHO 3 is ulceration, pain requiring analgesics, feeding direct contact with the mucosa.
is impossible and WHO 4 is necrosis, total parenteral The patients performed oral hygiene before the
nutrition. applications. The patients and the operator (VYK) wore
The OMAS scale measures ulceration and ery- protection eyeglasses during the procedure, which was
thema. The assessment for ulceration in each site was carried out by the bedside on the ward, with the patient
scored from 0-3, with 0 representing no clinical lesion, being isolated. Before the irradiations, the active tips
1 representing an ulcer <1 cm2, 2 representing an ulcer of the pens were disinfected with 70% alcohol and
of 1-3 cm2, and 3 representing an ulcer >3 cm2. The covered with PVC film to avoid cross-contamination
erythema was scored between 0-2, with 0 represent- and at the end the PVC cover was discarded and the tip
ing no erythema, 1 representing mild to moderate and was disinfected again. The applications were performed
2 representing severe erythema. The sites of the oral up to D+15, coinciding or not with engraftment of
mucosa evaluated with the OMAS scale were: upper hematopoietic stem cells. If engraftment was observed
and lower lips (vermilion and mucosa), bilateral jugal before this day, the irradiations were stopped in order
mucosa, floor of the mouth, lateral tongue surface on not to impair the study.
both sides, and ventral surface of the tongue, to which Data were analyzed by the non-parametric Wil-
therapeutic laser was applied in group I. According to coxon test for 2 independent samples, with the level
the OMAS criteria, the OMAS score = 2.5 x [(∑ui/3nu) of significance set at p<0.05. The exact version of the
+ (∑ei/2ne)] was applied, with values between 0 and 5. Wilcoxon test was used. Graphs were constructed using
∑ui is the total sum of ulceration, nu corresponds to the the Microsoft Office Excel 2003 and GraphPad Prisma
number of areas with ulceration, ∑ei is the total sum of 4 and 5 softwares (GraphPad Software, Inc., San Diego,
erythema, and ne corresponds to the number of areas CA, USA).
with erythema, according to Sonis et al. (19).
After discharge from the wards, a specific ques- RESULTS
tionnaire about laser therapy was applied to group I to
check if they had any lesion, oral pain, swallow pain and The results obtained with the application of the

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218 V.Y. Khouri et al.

WHO scale are presented in Figure 1. Comparison of 75% reported not requiring analgesics for oral pain, 25%
the course of OM between patients of groups I and II, reported use the analgesics to oral pain, 100% pain to
showed that group I presented a lower frequency of OM swallowing, 100% improvement after laser applications.
(Fig. 1) and the difference between groups was statisti-
cally significant (p=0.02). DISCUSSION
The mean grade of mucositis observed in group I
was 1.75 ± 0.45, whereas group II presented a mean of OM is the most common and uncomfortable
2.45 ± 0.93. The difference between groups was statisti- adverse effect in patients subjected to high doses of
cally significant (p<0.01), according to the WHO scale. chemotherapy or radiotherapy and in patients subjected
Regarding the size of ulcerations in the oral cavity as a to HSCT. The clinical consequences are presence of pain
whole, group I presenting fewer sites with ulcerations/ and difficulty in feeding, swallowing and speaking (17).
pseudomembranes and a smaller number of lesions Several therapies for the prevention and treatment
compared to group II (Fig. 2). of OM have been tested, The most recent one was the
Using the OMAS scale, the mean frequencies use of palifermin (human recombinant keratinocyte
of OM observed in groups I and II were 7.0 ± 3.2 and growth factor, KGF), which stimulates epithelial cells.
14.0 ± 8.3, respectively, with statistically significant The results were significant, with reduction of both the
difference (p=0.01) between the groups. Figure 3 illus- incidence and the duration of severe OM, and improve-
trates the maximum OM values (ulceration + erythema) ment of pain (5).
according to the OMAS score. It can be seen that the Some therapeutic agents have shown insufficient
same values were obtained when laser therapy was used evidence in the literature regarding the prevention and/
and the results were statistically significant (p=0.026). or treatment of mucositis, such as chlorhexidine (preven-
There was no clinical difference in the manifestation tion), aminofostine (treatment), and chamomile (preven-
of erythema between groups, according to the OMAS tion and treatment), as reported by Rubenstein et al. (7).
scale. In group I, 10 patients presented mild/moderate Several studies have shown the benefits of thera-
erythema (83.3%) and mild/moderate to severe erythema peutic laser to prevent and treat oral mucositis and has
occurred in 2 patients (16.6%), while in group II, 8 pa- several biological effects such as pain relief, antiinflam-
tients presented mild/moderate erythema (80%), severe matory effects and acceleration of the regeneration of
erythema occurred in 1 patient (10%) and only 1 patient damaged tissues (10). Thus, laser therapy is a noninva-
this group did not present erythema (10%). sive technique that promotes pain relief and reduce the
Regarding the answers to the questionnaire ap- severity of oral mucositis in patients subjected HSCT,
plied to group I, 50% of the patients reported fewer le- as reported by Jaguar et al. (20).
sions, 10% more lesions, 40% did not show any lesions, The first studies in patients involved the use of
helium-neon (He-Ne) laser with a wavelength of 632.8

Figure 1. Frequency of oral mucositis in groups I and II (p=0.02). Figure 2. Size of the lesions in groups I and II.

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 Laser and oral mucositis 219

nm (9), while current studies use several types of diodes laser (685 nm) was used, 35 mW, 2 J/cm2 per point of
such as the InGaAIP laser of 660 nm (18), the InGaAlP application, and OM was graded according to National
laser of 685 nm (14) and 660 nm (12), the GaAlAs laser Institute’s Common Toxicity Criteria. The use of laser
of 830 nm (16). for prophylaxis showed reduction of mucositis in group
Eduardo et al. (18) reported the use of a InGaAIP 1 [8 patients (73%) presented OM grade 0] when com-
laser (660 nm) with 40 mW and energy density of 4 J/ pared to group 2 [2 patients (27%) had no OM]. The
cm2 (for prevention of ulceration) or 6 J/cm2 (for treat- use of laser for treatment in group III was done when
ment of confirmed ulcerations) in 30 patients undergoing OM was diagnosed and these patients noted pain relief
autologous (63.3%) or allogeneic (36.7%) HSCT. The and without oral mucositis worsening after laser.
results showed improvement of OM after laser therapy. In the present study, the group I was irradiated
According to Lopes et al. (14), laser treatment at several with AlGaInP (660 nm) and GaAlAs (780 nm) lasers
sites in the oral cavity during chemotherapy and radio- with 25 mW power, 6.3 J/cm2 dose, in 10 s time. The 2
therapy reduces the severity and duration of OM, oral lasers were used alternately from the start of the con-
pain and xerostomia. Antunes et al. (12) investigated the ditioning regimen until the D+15 post-transplantation.
use InGAlP laser (660 nm) with 50 mW and 4 J/cm2 for The WHO and OMAS scales were used for evaluating
prevention and reduction of OM in patients subjected to OM, according to Antunes et al. (12).
autologous or allogeneic HSCT. The WHO and OMAS Comparison of the course of OM between the use
scales were used simultaneously for the evaluation of to therapeutic laser (group I) and “Mucositis Formula”
mucositis in the oral cavity. The result was a reduction (group II) showed that group I presented a lower fre-
of the progression of the OM with better pain control quency and severity of OM, according to WHO scale.
with laser therapy. With the application of the OMAS scale, 33.30% patients
The use of laser therapy can be a powerful in- did not show any lesions and 66.60% showed lesions of
strument to reduce of mucostis in patients undergoing <1 cm2, whereas group II developed a major frequency
chemotherapy. In a pilot clinical study (13), the pediatric of OM and more extensive lesions.
patients were randomized to group I (prophylactic laser The use of therapeutic laser in the present study
irradiation), group II (placebo laser irradiation) and showed positive outcomes and the efficacy of laser to
group III (therapeutic laser irradiation). The AsGaAl prevent and treat OM in patients subjected to HSCT,
chemotherapy and radiotherapy, in accordance with data
found in the literature (8,11-16,18,20) and the results
were similar to those obtained by Antunes et al. (12).
The outcomes of the present study add to the evidence
that therapeutic laser can be an effective option for the
prevention and treatment of OM in patients subjected to
HSCT with the absence of adverse effects or discomfort,
as suggested by other authors (11,13).
However, few patients have been treated and
most studies are not randomized. Thus, further studies
with therapeutic laser on patients susceptible to OM are
needed, preferably using a larger population. Neverthe-
less, in order to avoid conflicting results, it is necessary
to standardize irradiation protocols for patients subjected
to high doses of chemotherapy, followed or not by BMT.
The availability of specialized professionals qualified
for the use of laser according to safety guidelines is of
paramount importance.
In conclusion, in the present study, patients
treated with low-level laser therapy (group I) presented
Figure 3. Evaluation of the severity of oral mucositis according a lower frequency and progression of OM than those
to the OMAS score (p=0.026).

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220 V.Y. Khouri et al.

that received conventional therapy with the “Mucositis   5. Spielberger RT. Kepivance™: a breakthrough for oral mucositis
associated with mieloablative hematopoietic stem cell transplanta-
Formula” (group II). The inclusion of laser therapy also tion. Center Int Blood Marrow Transplant Res 2005;11:1-12.
reduced the number and severity of the lesions in patients   6. Massacesi C. Cancers therapy-induced oral mucositis: a compre-
of group I with established OM compared to group II. hensive review. Oncol 2005;2:1-12.
The present results add important evidence regarding   7. Rubenstein EB, Peterson DE, Schubert M, Keefe D, Mcguire D,
Epstein J, et al.. Clinical practice guidelines for the prevention
the use of laser therapy as a standard method for the and treatment of cancer therapy-induced oral and gastrointestinal
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  8. Campos L, Simões A, Sá HRN, Eduardo CP. Improvement in qual-
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  9. Bensadoun RJ, Ciais G. Radiation-and chemotherapy-induced
A mucosite oral (MO) afeta pacientes que são submetidos ao mucositis in oncology: results of multicenter phase III studies. J
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e a evolução da MO entre os pacientes submetidos ao laser laser therapy on iNOS expression using bioluminescence imaging.
terapêutico e da terapia convencional (uso de solução de bo- Photochem and Photobiol 2005;81:1351-1355.
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laser AlGaInP (660 nm) e laser GaAlAs (780 nm), potência de
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25 mW, dose de 6,3J/cm2, tempo 10 s, seguido do tratamento
Mayhe R, et al.. Low power laser in the prevention of induced oral
convencional; grupo II submetido apenas ao tratamento conven- mucositis in bone marrow transplantation patients: a randomized
cional. Ambas as escalas da World Health Organization (WHO) trial. Blood 2006:1-22.
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para avaliar os resultados. Os dados foram analizados pelo teste Caran EM, et al.. Low-level laser therapy in the prevention and
não-paramétrico de Wilcoxon, com p<0,05 considerado estatis- treatment of chemotherapy-induced oral mucositis in young pa-
ticamente significante. O grupo I apresentou menor frequência tients. Photomed Laser Surg 2008;26:394-400.
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Maurício Navarro Barros and Dr. Renato Luiz Guerino Cunha 17. Scully C, Sonis S, Diz PD. Mucosal diseases series: oral mucositis.
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Accepted August 11, 2009

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