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K E Y W O R D S Background: Observing and recording the signs and symptoms of oral mucositis
Adolescence are an important part of oral care, essential to the prevention and treatment of
Children mucositis. Structured oral assessment enables a more informed and accurate
Mucositis measurement identification of signs and symptoms and will enable early and individualized
Oral mucositis interventions. Objective: A United KingdomYbased mouth-care group
Review conducted a systematic review of the published literature through to March 2004
Systematic and repeated in 2008. The goal of this review was to identify and evaluate the range
of instruments used to assess oral mucositis to recommend in evidence-based
guidelines the ‘‘best’’ instrument to use in the field of children’s and young people’s
cancer care. Methods: Search sources included the Cochrane Library, MEDLINE,
EMBASE, and CINAHL. Studies were selected using defined criteria and reviewed
by 3 pairs of group members. Results: Fifty-four individual oral assessment
instruments were identified with only 15 reporting evidence of reliability and validity
testing. Only 3 articles reported on oral assessment exclusively in our population.
Author Affiliations: Great Ormond Street Hospital for Children NHS Correspondence: Faith Gibson, MSc, PhD, RSCN RGN Cert Ed RNT,
Trust and London South Bank University at Department of Children’s Nursing, FRCN, Department of Children’s Nursing, Faculty of Health & Social Care,
Faculty of Health & Social Care, London South Bank University London, London South Bank University, 103 Borough Rd, London SE10AA, UK
England (Dr Gibson); Manchester Children’s Hospitals, Pendlebury, Man- (Gibsof@gosh.nhs.uk; faith.gibson@lsbu.ac.uk).
chester, England (Ms Auld); School of Nursing Midwifery and Social Work, Accepted for publication November 12, 2009.
University of Manchester, Manchester, England (Ms Bryan); Paediatric
Oncology and Haematology, St James’s Hospital, Leeds, UK (Ms Coulson);
Evidence-Based Child Health Unit, Institute of Child Health, University of
Liverpool, Alder Hey Children’s NHS Foundation Trust, Liverpool, England
(Dr Craig); Evidence Based Oral Health Care, School of Dentistry, University of
Manchester, Manchester, England (Dr Glenny).
Written on behalf of the Children’s Cancer and Leukaemia Group and
Paediatric Oncology Nurses Forum Mouth Care Group.
The Children’s Cancer and Leukaemia Group is funded by a grant from
Cancer Research UK, and the ongoing work of the Mouth Care Group is
supported by CLICSargent.
T
reatment of childhood cancer is becoming increasingly mittee to look at mouth care and develop comprehensive
effective, with survival rates reported at 70% to 75% in evidence-based guidelines to aid decision making in this area.
parts of Europe and North America.1 Despite advances These guidelines aim to establish the most effective oral care
in chemotherapy and radiotherapy, cancer treatment remains as- strategies, as indicated by the best available research evidence.
sociated with clinically important, sometimes treatment-limiting, As part of the development of these guidelines, a systematic
adverse effects. Oral mucositis is a common consequence of review was conducted to determine the evidence relating to
treatment, occurring in approximately 30% to 75% of patients, methods of oral assessment. This review will present the process
depending on treatment type.2,3 In about 50% of patients with undertaken to identify and evaluate the range of instruments
mucositis, lesions can be severe causing significant pain, in- used to assess oral mucositis to recommend the ‘‘best’’’ in-
terfering with nutrition, and sometimes requiring modification strument to use in the field of children’s and young people’s
of the chemotherapy regimen. In addition, mucositis may pre- cancer care.
dispose a child to fungal infection (most commonly candidiasis),
viral infection (eg, herpes simplex virus), and bacterial infection,
which may lead on to life-threatening systemic infection. This n Materials and Methods
sequel of cancer treatment is important as it can impact severely
on a patient’s quality of life4 and may limit delivery of cancer A guideline development panel, constituting members of the
treatment.5 Oral complications remain one of the most chal- CCLG-PONF Mouth Care Group, was established. This in-
lenging cancer-related symptoms to manage. cluded pediatric oncologists, dentists, pediatric oncology nurses,
Observing and recording the signs and symptoms of oral a dental hygienist, a statistician, and research methodologists
mucositis are an important part of oral care that are essential to with experience in systematic reviews. The guidelines were de-
the prevention and treatment of mucositis.6,7 Structured oral veloped, where possible, following methods outlined by the
assessment enables a more informed and accurate identification Scottish Intercollegiate Guidelines Network (SIGN).15 Initially,
of signs and symptoms and will enable early and individualized a consensus approach was used to establish the scope and basic
interventions that may decrease the risk of secondary problems structure of the guidelines. Three key areas were addressed
such as septicemia and pain.8Y10 In addition, the effectiveness of within the guidelines: methods of oral assessment, dental care
interventions can be clearly articulated when ongoing assess- and basic oral hygiene, and drugs and therapies.
ment is central to an oral care protocol.9 Better defining oral Only the review pertaining to the methods of oral assess-
assessment can also help clarify terminology and provide ac- ment will be detailed in this article. A report describing the
curate descriptions of a child’s oral status. Structured symptom development of the guidelines in general is available.16
assessment has shown to result in health professionals having a
greater awareness of patients’ experience of cancer-related symp-
Preliminary Search
toms.11 Yet, in a telephone survey conducted by the authors of
this article, only 16 of the 22 UK Children’s Cancer and An initial search was undertaken for 3 reasons: to gain an
Leukaemia Group (CCLG) centers reported using an oral as- overview of the volume of literature, to inform the research
sessment scale. Assessment was primarily undertaken by nursing questions, and to establish the research methodologies used
staff.12 Although there is evidence supporting the benefits of within the area. This search did not seek to identify all relevant
systematic examination of oral status, the use of oral assessment information but aimed to provide the basis on which to make
instruments has failed to be universally implemented into certain organizational and methodological decisions with re-
clinical practice. gard to the guideline development process. The search was run
Clinical guidelines have been viewed as a way of helping to on MEDLINE (OVID Biomed 1966 to January 2002).
promote research-based practice, thus encouraging clinical prac- Seventy-eight records were identified and distributed to the
tice to be based on relevant, scientifically rigorous research evi- assessment subgroup of the guideline panel. This subgroup
dence.13,14 The CCLG and the Paediatric Oncology Nursing liaised by e-mail/telephone to formulate a list of questions to be
Forum (PONF) of the United Kingdom established a subcom- addressed in the guidelines. These questions were circulated to
While many of the calculations were straightforward and hence developed for use in stem cell transplant patients, but unlike
would be described as easy to use, 4 instruments required com- the Stiff et al instrument, the Kushner et al54 instrument asks
plex calculations to be carried out, precluding the instrument patients to recall the condition of their mouth over the
from use in everyday clinical practice.33,69,70,72 One tool used a previous week. The instrument of Öhrn and colleagues61 also
set of complex grading rules to assign a grade,59 limiting the use uses VASs to ask 10 questions about the patient’s level of pain,
of this instrument in everyday clinical practice and necessitating mouth dryness, salivary viscosity, ability to talk and perform
extensive training of personnel prior to its use in research. While oral hygiene, dysphagia, taste alterations, the condition of the
we recognize that the future development of targeted growth lips and gingiva, and whether the patient feels he/she has a
factors may well necessitate more complex assessment of mu- clean mouth. This instrument has been used weekly alongside
cosal injury, this instrument59 in its current format would not the Oral Mucositis Index66 in a mixed sample of chemo-
be considered the instrument of choice in children’s cancer therapy and radiotherapy patients.61
care because of its complexity and its reliance on sustained Fifteen studies were identified as providing some assessment
observation of the oral cavity. of the quality of the instruments through a process of validity
Three instruments were identified reporting entirely patient- and/or reliability testing.39,45,46,48,51,54,59,64,69Y72,74,77,78 One
generated scores.54,61,71 Stiff and colleagues71 developed the instrument could not be assessed for validity and reliability
Oral Mucositis Daily Questionnaire to assess the impact of because of the initial source being unavailable and the related
mucositis on pain and daily functioning in patients undergoing article having no validity information.36 An evaluation of these
stem cell transplantation. This is composed of 6 questions, studies, using an adaptation of the SIGN Diagnostic Studies
including 3 visual analog scales (VASs), and asks patients about Checklist,15 is presented in Table 2. Seven studies avoided
their overall oral health, the amount of mouth and throat selection bias by either enrolling consecutive series of patients
soreness they have experienced over the previous 24 hours, and or patients chosen at random from a suitable popula-
whether this soreness had limited any of 5 daily activities tion39,46,48,64,69,71,74 All except one of the studies was felt to
(swallowing, talking, eating, drinking, and sleeping). The final include participant’s representative of those on whom the test/
2 questions concern patient reports of diarrhea.71 The instru- assessment instrument would be used. This study involved
ment of Kushner and colleagues54 uses VASs to record patient only adults receiving hematopoietic stem cell transplant but
reports. Ten questions are asked about mouth pain; restriction suggests that further testing should be carried out with patients
of speech; difficulty eating (hard foods, soft foods); difficulty receiving other forms of therapy.64
in, and restriction of, drinking due to mouth sores; difficulty With regard to the validity of instruments assessed, only 6
in swallowing; and taste changes. This instrument was also studies reported on face validity (whether an instrument appears
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
degrees of erythema,
ulceration, pain, and
ability to eat
continues
Gibson et al
Hard/
Mucous Soft Swallow/ Self- Dry
Lips Tongue Membrane Gingiva Teeth Palate Saliva Voice Dysphagia Taste Diet care Pain Mouth Comments
38
Chapko et al ¾ Part of behavioral measure
of mouth pain, nausea,
and well-being
No compound score
Chen et al39 ¾ ¾ ¾ ¾ ¾ ¾ ¾ ¾ Assessing usability of Eilers’
OAG with children
Each component graded 1Y3
Compound score (8Y24)
Cox and Pajak40 ¾ Part of RTOG/EORTC
(RTOG/ late radiation scoring
EORTC) scheme
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Reports difficulties in
monitoring change
Eilers et al ¾ ¾ ¾ ¾ ¾ ¾ ¾ ¾ Each component graded 1Y3
E7 n
continues
Table 1 & Components Covered in Identified Oral Assessment Tools, continued
Hard/
Mucous Soft Swallow/ Self- Dry
Lips Tongue Membrane Gingiva Teeth Palate Saliva Voice Dysphagia Taste Diet care Pain Mouth Comments
Developed for research use
and clinical practice
Ferretti et al49 ¾ ¾ ¾ Signs used to grade
mucositis (0Y3)
Gandemer et al50 ¾ ¾ ¾ ¾ ¾ ¾ ¾ ¾ Anatomical sites graded
0Y3, functional signs
graded 0Y2, pain VAS
0Y100. Interim
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
(mOMAS)54 replaced with 100-mm
VAS scales for erythema
and ulceration at each
site. Total erythema and
Gibson et al
continues
Hard/
Mucous Soft Swallow/ Self- Dry
Lips Tongue Membrane Gingiva Teeth Palate Saliva Voice Dysphagia Taste Diet care Pain Mouth Comments
total oral ulceration also
graded using VAS
Lievens et al55 ¾ ¾ Part of broader toxicity scale
Mucositis graded 0Y6,
dysphagia graded 0Y4
No compound score
Lindquist et al56 ¾ ¾ ¾ ¾ ¾ ¾ ¾ Signs used to grade
mucositis (0Y3)
Maciejewski et al57 ¾ ¾ Each sign (within component)
(Dische system) graded 0Y3 or 0Y4
Compound score (0Y24)
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Compound score (0Y18)
Includes patient-reported
outcomes
E9
Table 1 & Components Covered in Identified Oral Assessment Tools, continued
Hard/
Mucous Soft Swallow/ Self- Dry
Lips Tongue Membrane Gingiva Teeth Palate Saliva Voice Dysphagia Taste Diet care Pain Mouth Comments
65
Raether et al ¾ ¾ ¾ ¾ Percentage of ulceration
Compound score
Schubert et al ¾ ¾ ¾ ¾ Structured according to signs
(OMI)66 rather than components
Includes patients based
assessment
Compound score
(maximum 34)
Kolbinson et al ¾ ¾ ¾ ¾ ¾ ¾ ¾ Developed as research tool
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Stiff et al71 ¾ ¾ ¾ Oral Mucositis Daily
QuestionnaireVpatient-
reported questionnaire;
continues
Gibson et al
Hard/
Mucous Soft Swallow/ Self- Dry
Lips Tongue Membrane Gingiva Teeth Palate Saliva Voice Dysphagia Taste Diet care Pain Mouth Comments
6 questions, 3 scored
0Y10, 3 scored 0Y4.
Used in conjunction with
WHO, RTOG, and
WCCNR within RCT.
No compound score
Sung et al72 ¾ ¾ ¾ ¾ ¾ ¾ Assessing usability of Sonis’
OMAS with children
Each component graded
Compound scoreV
weighted mean mucositis
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
(WCCNR, Bleeding and erythema
2004) also scored. Updated
n
mouth scores removed
continues
E11
Mucositis Index; OMRS, Oral Mucosa Rating Scale; PROMS, Patient-Reported Oral Mucositis Symptom; RTOG, Radiation Therapy Oncology Group; WCCNR, Western Consortium for Cancer Nursing Research;
Abbreviations: CALGB, Cancer and Leukaemia Group B; EORTC, European Organisation for Research and Treatment of Cancer; OAG, Oral Assessment Guide; OMAS, Oral Mucositis Assessment Scale; OMI, Oral
inherent problems with instruments being used in children,
No compound score
Used to inform oral
Comments
hygiene regimen
instrument items may not be sufficiently sensitive to
Compound score
mouth status
score (0Y21)
discriminate important differences between groups or detect
changes over time.93 If changes are expected to be very small,
an instrument must be sensitive to detect changes. In
addition, there is value in grounding measurement in the
experience of knowledgeable informants, a process that might
influence sensitivity. Of those studies detailing use and testing of
Mouth
Dry
¾
be assessed,94 based on what is important, relevant, and
discriminating in terms of oral mucositis. For example, content
Self-
care
children, where the order of the items was altered, and placing
¾
OAG.51
¾
Palate
Soft
WHO81Y83
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Do you feel the Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y
tool appears to
n
continues
E13
Table 2 & Assessment of Studies, Using Adapted Diagnostic Studies Checklist,15 Reporting Validity/Reliability Testing of Oral Assessment Tools, continued
Chen Dibble Donnelly Eilers Gibson Kushner McGuire Olson Potting Sonis Spijkervet Stiff Sung Tardieu WCCNR
et al39 et al45 et al46 et al48 et al51 et al54 et al59 et al78 et al64 et al69 et al70 et al71 et al72 et al74 et al77
(2004) (1996) (1992) (1988) (2006) (2008) (2002) (2004) (2005) (1999) (1988) (2006) (2006) (1996) (1991)
condition of Y
the mouth?
Was content Y Y N Y Y N Y N Y Y N N N N Y
validity
reported?
Were appropriate Y Y V Y Y V Y V Y Y V V V V Y
experts
consulted in
the
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
measured
independently
(blind) of
each other?
Gibson et al
Chen Dibble Donnelly Eilers Gibson Kushner McGuire Olson Potting Sonis Spijkervet Stiff Sung Tardieu WCCNR
et al39 et al45 et al46 et al48 et al51 et al54 et al59 et al78 et al64 et al69 et al70 et al71 et al72 et al74 et al77
(2004) (1996) (1992) (1988) (2006) (2008) (2002) (2004) (2005) (1999) (1988) (2006) (2006) (1996) (1991)
Was the choice V V V V V Y U U V V Y V V V U
of patients for
assessment by
the reference
standard
independent
of the test’s
results?
Was the V V V V V U U U V V U V V V Y
reference
standard
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
children?
Would you use Y Y N Y N N Y N Y N N Y N N N
n
continues
E15
of a composite score, as opposed to scoring individual items was
WCCNR
Table 2 & Assessment of Studies, Using Adapted Diagnostic Studies Checklist,15 Reporting Validity/Reliability Testing of Oral Assessment Tools, continued
(1991)
et al77
also considered by Gibson and colleagues.51 Although the final
N
decision was to continue to refer to a total score, its inter-
pretation into clinical practice is based on an individual item
Tardieu
(1996)
et al74
score, where interventions are guided by a treatment algorithm
N
focused on individual items contained in the instrument.99
There was little evidence in this review regarding the
validation of instruments, with only 15 of the identified 54
(2006)
et al72
Sung
N
instruments (28%) reporting psychometric testing to assess the
properties of validity or reliability (Table 2). As reliability will
vary from sample to sample, an instrument’s reliability should
(2006)
et al71
Stiff
(1988)
(2002)
et al59
(2008)
et al54
(2006)
et al51
(1992)
et al46
this tool in
children?
research
Oral Assessment Instruments Cancer NursingTM, Vol. 33, No. 4, 2010 n E17
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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Oral Assessment Instruments Cancer NursingTM, Vol. 33, No. 4, 2010 n E19
Copyright @ 2010 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.