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Original article

Trismus, xerostomia and nutrition status in

nasopharyngeal carcinoma survivors treated with radiation
Y.-J. CHEN, RN, MS, School of Nursing, College of Medicine, National Taiwan University, Taipei, S.-C. CHEN, RN,
PHD, ASSOCIATE PROFESSOR, Department of Nursing, Chang Gung University of Science and Technology, Taoyuan,

C.-P. WANG, MD, PHD, ASSOCIATE PROFESSOR, Department of Medicine, College of Medicine, National Taiwan Univer-
sity, Taipei, Y.-Y. FANG, RN, MS, School of Nursing, College of Medicine, National Taiwan University, Taipei,
Y.-H. LEE, RN, PHD, ASSISANT PROFESSOR, School of Nursing, College of Medicine, National Taiwan University, Taipei,
P.-J. LOU, MD, PHD, PROFESSOR, Department of Medicine, College of Medicine, National Taiwan University,
Taipei, J.-Y. KO, MD, PHD, PROFESSOR, Department of Medicine, College of Medicine, National Taiwan University,
Taipei, C.-C. CHIANG, RN, MS, Department of Nursing, National Taiwan University Hospital, Taipei, & Y.-H. LAI,
RN, PHD, PROFESSOR, School of Nursing, College of Medicine, National Taiwan University, Taipei, Taiwan

CHEN Y.-J., CHEN S.-C., WANG C.-P., FANG Y.-Y., LEE Y.-H., LOU P.-J., KO J.-Y., CHIANG C.-C. & LAI
Y.-H. (2014) European Journal of Cancer Care
Trismus, xerostomia and nutrition status in nasopharyngeal carcinoma survivors treated with radiation

The aims of the study were to: (1) examine levels of trismus, xerostomia and nutritional status; (2) compare
levels of trismus, xerostomia and nutritional status in patients with nasopharyngeal carcinoma (NPC) receiv-
ing different types of radiation modalities; and (3) identify factors related to NPC survivors’ risk status for
malnutrition and existing malnutrition. A cross-sectional study with consecutive sampling was conducted.
NPC survivors were recruited from otolaryngology/oncology outpatient clinics in a medical centre in Northern
Taiwan. Study measures included (1) Mandibular Function Impairment Questionnaire, (2) Xerostomia Ques-
tionnaire, (3) Mini Nutrition Assessment, (4) Hospital Anxiety and Depression Scale – Depression subscale,
and (5) Symptom Severity Scale. A total of 110 subjects were recruited. Those receiving intensity-modulated
radiation therapy had less trismus and xerostomia than patients receiving two-dimensional radiation therapy.
Patients with female gender, advanced stage, completion of treatments within 1 year, higher levels of depres-
sion, more severe trismus and higher symptom severity tended to have malnutrition or were at risk of
malnutrition. Trismus and xerostomia are long-term problems in some NPC survivors and may contribute to
malnutrition. To better manage a patient’s trismus and xerostomia and to enhance nutritional status, clini-
cians should develop a patient-specific care programme based on careful assessment and targeted measures to
improve oral function and insure adequate nutritional intake.

Keywords: nasopharyngeal carcinoma, nutrition, trismus, xerostomia, complication.

INTRODUCTION
Correspondence address: Yeur-Hur Lai, School of Nursing, College of
Nasopharyngeal carcinoma (NPC) is a geographically
Medicine, National Taiwan University, 1 Jen-Ai Road, Sec. 1 Taipei, 100,
Taiwan (e-mail: laiyhwk@ntu.edu.tw). linked cancer with high incidence in Southeastern China,
Conflicts of interest: None declared. Hong Kong and Taiwan (Jeyakumar et al. 2006). In
Accepted 22 October 2014 Taiwan, approximately 1500 new NPC cases are reported
DOI: 10.1111/ecc.12270 per year (Health Promotion Administration 2013).
European Journal of Cancer Care, 2014 Radiation therapy (RT) and concurrent (concomitant)

© 2014 John Wiley & Sons Ltd

CHEN ET AL.
chemoradiation therapy (CCRT) are recognised as the
most effective treatment modality to control local recur-
rence and prolong survival time (Pignon et al. 2000). The
3-year overall survival rate was 92.16% and 5-year overall
survival rate was 67.1% to 81.6% in NPC patients
without distant metastases (Qi et al. 2011; Peng et al.
2012; Chen et al. 2013).
Promising survival times also increase the challenges
of confronting delayed and long-term RT or CCRT-
related complications such as trismus (limited mouth
opening) and xerostomia (dry mouth) which may occur
during the initial 3 months of treatment up to a period of
several years (Cooper et al. 1995; Baharudin et al. 2009;
Kamstra et al. 2011; Deboni et al. 2012). Trismus occurs
in 5–38% of head and neck cancer patients and may
reduce the mouth’s opening by 18% after RT (Dijkstra
et al. 2004, 2006). This complication may compromise
normal oral intake and cause malnutrition problems,
and is identified as one of the major problems for head
and neck cancer patients (Kiyomoto 2007; Chasen &
Bhargava 2009; Jager-Wittenaar et al. 2011; Kamstra et al.
2011).
Comparison of the treatment effects between/among
different RT modalities has been the major focus of
research in past studies of patients with NPC (Fang et al.
2007; Su et al. 2012). Trismus (Abendstein et al. 2005;
Cohen et al. 2005; Oates et al. 2007; Chen et al. 2011), dry
mouth (Brizel et al. 2000; Abendstein et al. 2005; Oates
et al. 2007; Rogers et al. 2009; Wang et al. 2011; Marucci
et al. 2012) and nutrition status (Logemann et al. 2003;
Larsson et al. 2005; Oates et al. 2007; Buijs et al. 2010)
were generally viewed and assessed as part of quality of
life issues (Abendstein et al. 2005; Garcia-Peris et al.
2007; Oates et al. 2007; Rogers et al. 2009; Marucci et al.
2012). In studies often limited to traditional acute treat-
ment directed care and medical payments, delayed or
long-term RT or CCRT complications did not receive
sufficient attention. In head and neck cancer patients,
nutrition dysfunction (malnutrition) is another problem
potentially linked to the consequences of oral complica-
tions. Related factors should be considered in attempts to
improve head and neck cancer (HNC) patients’ malnutri-
tion problems.
Based on previous investigations, factors considered
include treatments (modalities of RT and time since com-
pleting treatments) (Vissink et al. 2003a,b; Agulnik &
Epstein 2008; Elting et al. 2008; Rosenthal et al. 2008; Wu
et al. 2011), and general symptom severity or delayed
problems (trismus and dry mouth) (Garcia-Peris et al.
2007). Psychological distress, such as depression, may
also diminish patients’ willingness to eat (Bodnar &
2 © 2014 John Wiley & Sons Ltd
Wisner 2005; Rao et al. 2008; Haisfield-Wolfe et al. 2009;
Capuano et al. 2010; Howren et al. 2010; Kim et al. 2011;
Britton et al. 2012). There is limited research that simul-
taneously examines these factors and their influence
related to malnutrition in NPC survivors. The aims of
the study were to: (1) examine the levels of trismus,
xerostomia and nutritional status in survivors of NPC
after RT or CCRT; (2) compare the levels of trismus,
xerostomia and nutritional status in survivors treated
with different modalities of RT; and (3) identify factors
related to survivors who are at risk of malnutrition. In
this study, survivors were defined as those patients alive
and continuing to function at the time of diagnosis or
after completing treatment (National Cancer Insititute
2013).
METHODS
Design
This is a cross-sectional study with consecutive sampling
in a medical centre in Taiwan. Eligible patients were
those (1) diagnosed with NPC who had completed RT or
CCRT for at least 3 months up to 5 years; (2) disease-free
survivors, patients who did not show apparent signs of
cancer recurrence; (3) who agreed to participate in the
study after being informed of the purposes by research
nurses; and (4) who could communicate verbally or in
writing.
According to the treatment guidelines of NPC, patients
received RT within 6 to 7 weeks. The RT doses was
2.0–2.12 Gy per fraction per day, administered 5 days per
week with a total doses of approximately 70 Gy. Patients
who underwent CCRT received induction chemotherapy
or concomitant chemotherapy, with induction chemo-
therapy for locally advanced stages and concomitant
chemotherapy for stage II, III or IV (NCCN 2012).
Ethical considerations
Institutional review board approval was obtained from
National Taiwan University Hospital Research Ethics
Committee and patients provided written consent before
data collection.
Data collection
Consecutive patients were approached in the otolaryngol-
ogy and oncology outpatient departments at a medical
centre in northern Taiwan from January 2010 to Decem-
ber 2012 by a well-trained research nurse. The research
nurse briefly explained the purposes and procedures of this
 Nutrition, trismus and dry mouth in nasopharyngeal carcinoma patients
study before obtaining informed consent. Eligible patients
were interviewed using structured questionnaires by the
trained research nurse.
Instruments
Instruments used to assess patients were translated into
Chinese versions and are as follows:
Mandibular Function Impairment Questionnaire (MFIQ)
The severity of trismus was measured by the 17-item
MFIQ (Stegenga et al. 1993). It includes two subscales: (1)
limit while opening mouth (11 items) and (2) limit while
biting, chewing and swallowing foods (6 items). The MFIQ
is a 0 to 4 Likert-type scale with 0 representing ‘no distress
at all’ and 4 representing ‘very difficult or impossible
without help’. The total scores of MFIQ range from 0 to
68, with higher scores indicating more severe trismus.
The Cronbach’s alpha of the MFIQ in the current study
was 0.94.
Xerostomia Questionnaire (XQ)
The severity of dry mouth was assessed using the XQ. The
XQ is a 9-item self-report on an 11-point (0–10) numerical
scale. A standardised method was used to convert the
summed score into a 0–100 range for the total score with
higher scores indicating more severe dry mouth (Eisbruch
et al. 2001). Cronbach’s alpha for the XQ in this study was
0.92.
Mini Nutrition Assessment (MNA)
The MNA was used to assess patients’ nutritional status
and was composed of three major parts: anthropometric
measurement, general nutrition and dietary assessment
(Guigoz & Vellas 1997). The total scores of MNA ranged
from 0 to 30, with higher scores indicating better nutri-
tional status. Three types of nutrition status categorised
with cut-off points were: (1) undernourished (scores less
than 17), (2) at risk of undernourished (1723.5), and (3) well
nourished (24 or higher) (Tsai et al. 2010). Satisfactory
psychometric properties for MNA have been reported in
cancer-related studies in Taiwan (Tsai et al. 2009, 2010).
In the current study, Cronbach’s alpha was 0.73. Patients
at undernourished status and at risk of undernourished
were defined as ‘at a risk of malnutrition’ in the study for
further analysis.
Symptom Severity Scale (SSS)
The SSS was developed to assess cancer or treatment-
related common symptoms (Lai 1998). The 20-item SSS is
© 2014 John Wiley & Sons Ltd
a self-report 11-point (0–10) numerical scale, with 0 indi-
cating ‘no such symptom at all’ and 10 indicating ‘as
severe as I can imagine’. Satisfactory psychometric prop-
erties have been reported in a head and neck cancer-
related study in Taiwan (Chen et al. 2010). Cronbach’s
alpha was 0.79 in the present study.
Hospital Anxiety and Depression Scale (HADS) –
Depression subscale
The 7-item depression subscale of the HADS was used to
assess patients’ depression (Zigmond & Snaith 1983). The
total scores for depression subscale ranges from 0 to 21,
with higher scores indicating higher depression (Zigmond
& Snaith 1983). The scale has been found to be reliable in
head and neck cancer-related studies in Taiwan (Chen
et al. 2010). Cronbach’s alpha for the HADS-depression in
this study was 0.70.
Background information form
Background information was collected which included
demographic, disease and treatment-related data. Disease
and treatment-related variables included the cancer stage
based on American Joint Committee on Cancer staging
system (Edge et al. 2010), radiotherapy modalities, months
since completion of treatments and physical performance
status assessed by Karnofsky performance status (KPS).
KPS is an 11-point scale with scores ranging from having
full normal function (100%) to dead (0%) (Karnofsky et al.
1948). The KPS has been widely used in clinical cancer
studies in Taiwan (Tsai et al. 2007; Chen et al. 2009).
Data analysis
Descriptive statistics were used to analyse patients’ demo-
graphic data, clinical characteristics, trismus, xerostomia
and nutritional status (aim 1). Analysis of variance was
used to analyse the differences of trismus, xerostomia and
nutritional status among RT modalities (aim 2). General
symptom severity was composed of those symptoms/items
having mean scores higher than 2 (Chen et al. 2010). Any
item in SSS with a mean score higher than 2 was selected
and further formed the general symptom severity variable.
In the current study, six symptoms (items) with mean
scores higher than 2 were selected. Among the six items,
‘dry mouth’ had the highest mean score [mean (M) = 5.5,
standard deviation (SD) = 2.1]. Since the XQ was already
used as an indicator of xerostomia in the current study, we
did not incorporate this item (dry mouth) into the general
symptom severity. The general symptom severity scores
were formed by the average scores of the remaining five
3
CHEN ET AL.

symptoms which included swallowing difficulty, fatigue, Table 1. Demographic and disease characteristics of patients
insomnia, shoulder stiffness and taste change. To identify (n = 110)

the factors related to a risk of malnutrition, the NPC Characteristics n (%) Mean (SD)

survivors’ nutritional statuses were dichotomised as ‘with Age (years) 49.8 (11.2)
Gender
or without at a risk of malnutrition’. Nutrition status types
Male 80 (72.7)
for ‘undernourished (scores < 17)’ and ‘at risk of malnutri- Female 30 (27.3)
tion (17–23.5)’ were considered to indicate risk of malnu- Working status
trition, whereas nutrition status type for ‘well-nourished Retired 9 (8.2)
Lost job because of cancer 25 (22.7)
(≥24)’ was considered indicative of without risk of malnu- Part-time 10 (9.1)
trition (Guigoz & Vellas 1997). Logistic regression was used Full-time 58 (52.7)
to identify factors related to with or without a risk of Others 8 (7.3)
Months since the completion of 23.6 (18.7)
malnutrition (dependent variable) (aim 3). Independent
radiotherapy
variables were significant factors derived from Pearson’s Completion of treatments in 1 year 39 (35.5)
correlation and included age, physical performance status Completion of treatments for more 71 (64.5)
(KPS), gender (male vs. female), cancer stage (stage IV vs. III than 1 year
Cancer stage
vs. II vs. I), time since completion of treatment (more than
I 9 (8.1)
1 year vs. within 1 year), trismus, xerostomia, general II 20 (18.2)
symptom severity (five selected symptom items) and III 31 (28.2)
depression. However, there was no significant difference IV 50 (45.5)
Modalities of radiotherapy
between the types of chemotherapy in nutrition status (t = Tomotherapy 21 (19.1)
−1.81, P = 0.07), trismus (t = 0.92, P = 0.37) and xerostomia Intensity-modulated radiation 69 (62.7)
(t = 0.53, P = 0.60); therefore, chemotherapy was not therapy (IMRT)
3D radiation therapy 8 (7.3)
selected as a factor in the model analysis. The level of
2D radiation therapy 12 (10.9)
statistical significance was set at P < 0.05. Data were Radiotherapy (total doses, cGy) 6995.0 (44.1)
analysed by IBM SPSS version 21.0 (Armonk, NY, USA). Type of chemotherapy
Induction chemotherapy 23 (20.9)
Concomitant chemotherapy 87 (79.1)
RESULTS
Comorbidity
None 83 (75.5)
Subject characteristics
Hypertension 10 (9.1)
A total of 123 eligible patients were approached. There Diabetes 3 (2.7)
Heart disease 2 (1.8)
were 110 subjects who agreed to participate and who com- Others 12 (10.9)
pleted the interview in the study (response rate: 89.4%). Karnofsky performance score
Two patients refused to participate in the study and 11 80 23 (20.9)
patients failed to complete the whole interview. Of the 110 90 87 (79.1)

subjects in the study, 72.7% were male. The average age

was 49.8 (SD = 11.2) and approximately half of the patients
(52.7%) had full time jobs. The mean time to completion of
RT was 23.6 months (SD = 18.7), with a range of 3.0–60.8
months. Most patients were at stage III (28.2%) or stage IV
(45.5%); stage IV included T4, N0-2, M0 (stage IVa) (31.9%),
any T, N3, M0 (stage IVb) (12.7%), and any T, any N, M1
(stage IVc) (0.9%) (Edge et al. 2010). Our sample reflected
the typical distribution of NPCs in national ratios; approxi-
mately 70% of NPC patients were diagnosed at locally
advanced stage III or IV (Agulnik & Epstein 2008).
A majority of patients received intensity-modulated
radiation therapy (IMRT) (62.7%) with a mean total radia-
tion doses of 6995 cGy (SD = 44.1, range = 6600–7075).
Most patients (79.1%) received concomitant chemo-
therapy, with 68.2% receiving cisplatin, 6.4% receiving
cisplatin and fluoride (PF) and 4.5% receiving fluoride. A
total of 20.9% of patients received induction chemo-
therapy, with 17.3% receiving mitomycin, epirubicin,
cisplatin, fluoride and leucovorin, and 3.6% receiving
cisplatin and fluoride (PF). The majority of subjects
(79.1%) reported a good performance status with a KPS
score of 90 after completing treatment (Table 1).
Characteristics of trismus, xerostomia and
symptom severity
Patients’ trismus was assessed by MFIQ. Generally,
patients’ trismus problems were mild but there were still
more than half of the participants (58.2%) who experi-
enced varied levels of difficulty in chewing hard food.
Almost half of the patients (49.1%) reported varied levels

4 © 2014 John Wiley & Sons Ltd

 Nutrition, trismus and dry mouth in nasopharyngeal carcinoma patients
of difficulty in taking a large bite of food and 30% reported
difficulties in chewing resistant food. Difficulties involv-
ing social activities were reported by 16.4% of patients.
Patients’ xerostomia was assessed by the XQ. The
summed score of XQ was 48.4 (SD = 18.7) which indicated
a moderate level of xerostomia. The item with the highest
mean score (M = 6.9, SD = 2.6) was frequency of sipping
liquids to aid in swallowing food. Patients also reported
discomfort related to dry mouth during eating, chewing
food and when not taking food.
Patients’ general symptoms were assessed by the SSS
(0–10 scoring). We selected and ranked symptoms with
mean scores higher than 2 which were dry mouth (M = 5.5,
SD = 2.1), swallowing difficulty (M = 3.5, SD = 2.3), fatigue
(M = 2.8, SD = 2.0), insomnia (M = 2.5, SD = 2.6), shoulder
stiffness (M = 2.4, SD = 2.2) and taste change (M = 2.2,
SD = 2.1). For the purpose of the current study, we
excluded the dry mouth item when calculating the general
symptom mean score as 2.6 (SD = 1.4).
Trismus, xerostomia and nutritional status for patients
receiving different RT modalities
Levels of trismus, xerostomia and nutritional status
were analysed individually across four modalities of RT
[tomotherapy, IMRT, three-dimensional RT and two-
dimensional (2D) RT]. The results showed that patients
who received 2D-RT had significantly more severe
trismus (F = 2.71, P < 0.05) and xerostomia (F = 2.94, P <
0.05) than those who received tomotherapy and IMRT.
There were no differences in patients’ nutritional status
across different RT modalities. No statistically significant
differences were shown in RT doses among groups in four
RT modalities (Table 2).
Nutritional status and factors related to nutritional status
The overall mean score of MNA was 23.8 (SD = 3.0). The
distribution of the MNA scores revealed that 47 patients
Table 2. Trismus, xerostomia and nutrition status among patients with different RT modalities (n = 110)
a. Tomotherapy (n = 21) b. IMRT (n = 69)
Variables Mean (SE) Mean (SE)
Doses of radiotherapy (cGy) 6981.0 (19.1) 6996.9 (3.13)
Trismus† 7.0 (2.5) 8.0 (1.2)
Xerostomia‡ 42.3 (3.0) 41.1 (2.7)
Nutrition§ 23.8 (0.5) 24.1 (0.4)
Note: *P < 0.05.
†Measured by Mandibular Function Impairment Questionnaire (MFIQ), ranging from 0 to 68.
‡Measured by Xerostomia Questionnaire (XQ), ranging from 0 to 100.
§Measured by Mini Nutrition Assessment (MNA), ranging from 0 to 30.
2D-RT, two-dimensional radiation therapy; 3D-RT, three-dimensional radiation therapy; IMRT, intensity-modulated radiation
therapy; LSD, Least Significant Difference; n.a., non-significant.
© 2014 John Wiley & Sons Ltd
(42.7%) were at a risk of malnutrition (MNA 17–23.5) and
one patient (0.9%) was undernourished (MNA < 17). From
bivariate Pearson’s correlation analyses, patients’ nutri-
tional status was negatively associated with trismus,
xerostomia, depression and symptom severity, and posi-
tively related to physical performance status (KPS) (r =
−0.43, −0.27, −0.47, −0.29, 0.26 respectively).
While entering these bivariately significant factors
together with treatment-related factors into the logistic
regression to predict the ‘at a risk of malnutrition’, the
results showed female gender, late stage, completion of
treatments within 1 year, higher levels of depression,
more severe trismus and higher symptom severity.
For female patients and with stage IV cancer (vs. stage I),
the likelihood of being at risk of malnutrition was 11.6
times [95% confidence interval (CI): 2.92–46.29) and 16.2
times (95% CI: 1.098–238.602) higher than for patients
who were male and with stage I cancer respectively. For
patients having completed treatments within 1 year, the
likelihood of being at risk of malnutrition was 6.63 times
higher (95% CI: 1.64–26.77) than patients completing
treatments for more than 1 year. Patients’ risks, or odds
ratio (OR) for being at risk, of malnutrition were higher
when they reported higher levels of depression, trismus
and symptom severity. These patients’ OR increased
by 1.29 (95% CI: 1.05–1.60), 1.08 (95% CI: 1.02–1.15) and
1.97 (95% CI: 1.22–3.16) times respectively with each unit
increase in the scores (Table 3).
DISCUSSION
The present study examined the status and relationship of
trismus, xerostomia and nutritional status in NPC survi-
vors after RT or CCRT. Several important issues were
identified.
In our study, some NPC survivors reported mild to
moderate difficulties in mouth opening which was similar
to previous studies (Dijkstra et al. 2004, 2006). Our study
revealed that patients reported moderate levels of
c. 3D-RT (n = 8) d. 2D-RT (n = 12) Post-hoc
Mean (SE) Mean (SE) F (LSD)
7000.0 (6.3) 6995.0 (4.2) 1.05 n.a.
8.5 (3.3) 17.1 (3.3) 2.71* d > a, b
51.6 (4.5) 54.3 (9.6) 2.94* d > a, b
24.0 (1.2) 22.4 (0.9) 1.13 n.a.
5
CHEN ET AL.

Table 3. Logistic regression of significant factors related to risk of malnutrition (n = 110)

Factors Beta SE Odds ratio 95% CI P value
Constant −5.844 1.745 0.003 – 0.001
Trismus* 0.078 0.030 1.081 1.020–1.146 0.008
Symptom severity (severity of the top 5 symptoms)† 0.676 0.243 1.965 1.221–3.163 0.005
Xerostomia‡ −0.039 0.021 0.962 0.923–1.002 0.059
Disease stage IV (vs. stage I) 2.784 1.373 16.188 1.098–238.602 0.043
Depression§ 0.258 0.108 1.294 1.048–1.599 0.017
Completion of treatments within 1 year (vs. more than 1 year) 1.892 0.712 6.631 1.642–26.771 0.008
Female (vs. male) 2.453 0.705 11.626 2.920–46.293 0.001
*Measured by Mandibular Function Impairment Questionnaire (MFIQ).
†Measured by Symptom Severity Scale (SSS).
‡Measured by Xerostomia Questionnaire (XQ).
§Measured by Hospital Anxiety and Depression Scale (HADS)-Depression Subscale.

xerostomia after completion of RT which reflected sali-
vary gland dysfunction with xerostomia indicated as the
most devitalising delayed and long-term complication
after RT (Wang et al. 2011). Both trismus and xerostomia
were found to be significantly more severe in patients
receiving 2D-RT which supports the assumption that
2D-RT may cause more severe muscle fibrosis and
reduced saliva. Although 2D-RT is no longer a therapy of
choice for NPC patients, clinical healthcare professionals
should be aware that some patients may have received
2D-RT before the treatment guideline changed. For all
patients receiving RT in the head and neck areas, system-
atic assessments combined with early mouth opening
exercises are essential care for HNC patients.
When nutritional status was measured in our study,
more than half of NPC survivors were well nourished
(56.4%). It suggests that NPC patients generally have
acceptable nutritional status. This might be because
majority of our participants are at least 1 year after
completion of RT. For the 42.7% of patients at risk of
malnutrition and the 0.9% of poorly nourished patients,
nutrition condition is still a concern. Our results are rela-
tively better than the Jager-Wittenaar et al. (2011) study.
They found that 25% of patients within 3 months after
treatment, 13% at 3–12 months after treatment and 3% at
12–36 months after treatment had malnutrition problems.
The differences reflect time from completion of RT. It
suggests that patients’ poor nutritional status gradually
improved after completion of RT.
Factors related to malnutrition status included trismus,
symptom severity, depression, female gender and cancer
stage. Trismus is the most robust factor related to
patients’ malnutrition status. Trismus limits patients’
mouth opening levels and directly limits their intake.
Xerostomia approaches significance in relationship to
patients’ nutritional status. The relationship between
xerostomia and nutritional status is not as strong as the
relationship between trismus and nutritional status in
limiting patients’ intake possibly due to patients’ use of
saliva substitutes (water, artificial saliva and sugar-free
mints) to help their eating. Patients with advanced cancer
stage also reported malnutrition which may be due to
more complicated treatments and more severe physical
conditions that influence the abilities and motivation
related to food intake resulting in a decreased nutritional
status.
Similar to previous studies (Kiyomoto 2007; Chasen &
Bhargava 2009; Jager-Wittenaar et al. 2011; Kamstra et al.
2011), the severity of symptoms from the sum of the
patients’ top 5 symptoms (swallowing difficulty, fatigue,
insomnia, shoulder stiffness and taste change) were found
to be related to patients’ malnutrition status. Based on our
results, the above mentioned symptoms might be viewed
as clustered symptoms linked to patients’ nutrition intake
and need to be carefully assessed before providing care
designed to improve patients’ nutrition status.
Patients’ depression was significantly positively associ-
ated to malnutrition which is similar to the Britton et al.
(2012) study. This result strongly suggests that psycho-
logical factors play an important role in patients’ food
intake. Patients’ depressive mood may decrease their
desire to eat. Depression may be derived from an imbal-
ance in the brains’ neurotransmitters, low levels of sero-
tonin or tryptophan, which results in loss of appetite,
skipping meals and losing interest in eating or preparing
meals (Rao et al. 2008). Nutrition supplements, more flex-
ible eating strategies and psychological support and/or
therapy to help patients develop more positive moods may
integrate into the nutrition intake programme to increase
patients’ nutritional status.
Female gender is a significant factor related to patients’
nutrition status. This finding may be because women tend

6 © 2014 John Wiley & Sons Ltd

 Nutrition, trismus and dry mouth in nasopharyngeal carcinoma patients

to have a more depressive state (Bodnar & Wisner 2005;
Kim et al. 2011). There is still a lack of sufficient infor-
mation to explain this result. Future research is needed to
explore the cause–effect relationships among depression,
gender and nutrition status.
There were some limitations in this study. The cross-
sectional data collection nature may not allow an in-depth
understanding of the changes and developments in nutri-
tion level and related factors. Further research with a
longitudinal design will provide additional knowledge and
identify the efficacy of education intervention on trismus,
xerostomia and nutrition statuses. Limited to data collec-
tion criteria from 5 years after the completion of major
treatments, the incidences of trismus, xerostomia and
nutrition statuses in NPC patients might not reflect
patients who have completed major treatments for more
than 5 years. Further study to examine these problems and
their incidences should extend to NPC patients who have
completed their major treatments for more than 5 years.
Food intake and choices are very culturally linked. This
study was conducted in Taiwan and may not reflect other
cultures and food choices. A qualitative research approach
may increase the understanding of NPC patients’ eating
habits and experiences and how these relate to their nutri-
tional status. Additionally, an objective assessment from
healthcare providers or physicians will be considered in
characterising NPC survivors during the post-treatment
period in the future study. Finally, the analyses in this
study primarily focused on the effects of highly linked
RT complications. However, NPC patients had mostly
received CCRT. The effects from chemotherapy might not
be neglected. Although there is no significant difference
in trismus, xerostomia and nutrition statuses among
patients receiving types of chemotherapy regimen, the
possible effects of chemotherapy on trismus, xerostomia
and nutrition intake are not yet clear. Future studies
are suggested to further examine the possible effects or
mechanisms of chemotherapy on the mentioned compli-
cations in NPC patients with CCRT.
CONCLUSION
Our study provides information about trismus, xerostomia
and nutritional status in survivors of NPC. The overall
findings suggest that nutritional status after RT is a mul-
tifactorial experience that involves physical, psychologi-
cal, disease/treatment and gender-related factors. These
factors should be carefully assessed at the beginning of RT,
a care protocol developed and ongoing follow up should
occur to prevent oral dysfunction and malnutrition in
patients with NPC and head and neck cancers receiving
RT. Future research should examine the longitudinal
changes that occur during and after RT and test interven-
tions designed to prevent and decrease RT related long-
term oral dysfunction and nutrition problems.
ACKNOWLEDGEMENTS
The authors sincerely acknowledge the patients partici-
pated in the study. This study was partly supported by the
grant to Dr. Yeur-Hur Lai from Ministry of Science and
Technology (MOST) in Taiwan. The authors also thank
Patricia Stanfill Edens, PhD, RN, LFACHE (Life Fellow
in the American College of Healthcare Executives) for
English editing. The first two authors contributed equally
to this study.

REFERENCES improving mental health among supplemented nutrition in malnourished

Abendstein H., Nordgren M., Boysen M.,
Jannert M., Silander E., Ahlner-Elmqvist
M., Hammerlid E. & Bjordal K. (2005)
Quality of life and head and neck cancer:
a 5 year prospective study. Laryngoscope
115, 2183–2192.
Agulnik M. & Epstein J.B. (2008)
Nasopharyngeal carcinoma: current man-
agement, future directions and dental
implications. Oral Oncology 44, 617–
627.
Baharudin A., Khairuddin A., Nizam A. &
Samsuddin A.R. (2009) Evaluation of irra-
diated salivary gland function in patients
with head and neck tumours treated with
radiotherapy. The Journal of Laryngology
and Otology 123, 108–113.
Bodnar L.M. & Wisner K.L. (2005) Nutri-
tion and depression: implications for
childbearing-aged women. Biological
Psychiatry 58, 679–685.
Britton B., Clover K., Bateman L., Odelli C.,
Wenham K., Zeman A. & Carter G.L.
(2012) Baseline depression predicts
malnutrition in head and neck cancer
patients undergoing radiotherapy. Sup-
portive Care in Cancer 20, 335–342.
Brizel D.M., Wasserman T.H., Henke M.,
Strnad V., Rudat V., Monnier A.,
Eschwege F., Zhang J., Russell L.,
Oster W. & Sauer R. (2000) Phase III
randomized trial of amifostine as a
radioprotector in head and neck cancer.
Journal of Clinical Oncology 18, 3339–
3345.
Buijs N., van Bokhorst-de van der Schueren
M.A., Langius J.A., Leemans C.R., Kuik
D.J., Vermeulen M.A. & van Leeuwen
P.A. (2010) Perioperative arginine-
patients with head and neck cancer
improves long-term survival. The Ameri-
can Journal of Clinical Nutrition 92,
1151–1156.
Capuano G., Gentile P.C., Bianciardi F.,
Tosti M., Palladino A. & Di Palma M.
(2010) Prevalence and influence of mal-
nutrition on quality of life and perfor-
mance status in patients with locally
advanced head and neck cancer before
treatment. Supportive Care in Cancer 18,
433–437.
Chasen M.R. & Bhargava R. (2009) A
descriptive review of the factors con-
tributing to nutritional compromise in
patients with head and neck cancer. Sup-
portive Care in Cancer 17, 1345–1351.
Chen S.C., Tsai M.C., Liu C.L., Yu W.P.,
Liao C.T. & Chang J.T. (2009) Support
needs of patients with oral cancer and

© 2014 John Wiley & Sons Ltd 7

CHEN ET AL.
burden to their family caregivers. Cancer
Nursing 32, 473–481.
Chen S.C., Lai Y.H., Liao C.T., Lin C.C. &
Chang J.T. (2010) Changes of symptoms
and depression in oral cavity cancer
patients receiving radiation therapy. Oral
Oncology 46, 509–513.
Chen Y., Sun Y., Liang S.B., Zong J.F.,
Li W.F., Chen M., Chen L., Mao Y.P.,
Tang L.L., Guo Y., Lin A.H., Liu M.Z. &
Ma J. (2013) Progress report of a
randomized trial comparing long-term
survival and late toxicity of concur-
rent chemoradiotherapy with adjuvant
chemotherapy versus radiotherapy
alone in patients with stage III to IVB
nasopharyngeal carcinoma from endemic
regions of China. Cancer 119, 2230–
2238.
Chen Y.Y., Zhao C., Wang J., Ma H.L., Lai
S.Z., Liu Y., Han F., Lu L.X., Bao Y. &
Chen M. (2011) Intensity-modulated
radiation therapy reduces radiation-
induced trismus in patients with
nasopharyngeal carcinoma: a prospective
study with >5 years of follow-up. Cancer
117, 2910–2916.
Cohen E.G., Deschler D.G., Walsh K. &
Hayden R.E. (2005) Early use of a
mechanical stretching device to improve
mandibular mobility after composite
resection: a pilot study. Archives of
Physical Medicine and Rehabilitation
86, 1416–1419.
Cooper J.S., Fu K., Marks J. & Silverman S.
(1995) Late effects of radiation therapy in
the head and neck region. International
Journal of Radiation Oncology, Biology,
Physics 31, 1141–1164.
Deboni A.L., Giordani A.J., Lopes N.N.,
Dias R.S., Segreto R.A., Jensen S.B. &
Segreto H.R. (2012) Long-term oral
effects in patients treated with
radiochemotherapy for head and neck
cancer. Supportive Care in Cancer 20,
2903–2911.
Dijkstra P.U., Kalk W.W. & Roodenburg
J.L. (2004) Trismus in head and neck
oncology: a systematic review. Oral
Oncology 40, 879–889.
Dijkstra P.U., Huisman P.M. & patients treated for oral or oropharyngeal
Roodenburg J.L. (2006) Criteria for
trismus in head and neck oncology. Inter-
national Journal of Oral and Maxillofa-
cial Surgery 35, 337–342.
Edge S., Byrd D.R., Compton C.C., Fritz
A.G., Greene F.L. & Trotti A. (2010)
AJCC Cancer Staging Manual, 7th edn.
Springer, New York, USA.
Eisbruch A., Kim H.M., Terrell J.E., Marsh
L.H., Dawson L.A. & Ship J.A. (2001)
Xerostomia and its predictors following
parotid-sparing irradiation of head-and-
neck cancer. International Journal of
Radiation Oncology, Biology, Physics 50,
695–704.
8 © 2014 John Wiley & Sons Ltd
Elting L.S., Keefe D.M., Sonis S.T., Garden
A.S., Spijkervet F.K., Barasch A., Tishler
R.B., Canty T.P., Kudrimoti M.K. &
Vera-Llonch M. (2008) Patient-reported
measurements of oral mucositis in head
and neck cancer patients treated with
radiotherapy with or without chemo-
therapy: demonstration of increased fre-
quency, severity, resistance to palliation,
and impact on quality of life. Cancer 113,
2704–2713.
Fang F.M., Tsai W.L., Chen H.C., Hsu H.C.,
Hsiung C.Y., Chien C.Y. & Ko S.F. (2007)
Intensity-modulated or conformal radio-
therapy improves the quality of life of
patients with nasopharyngeal carcinoma:
comparisons of four radiotherapy tech-
niques. Cancer 109, 313–321.
Garcia-Peris P., Paron L., Velasco C., de la
Cuerda C., Camblor M., Breton I.,
Herencia H., Verdaguer J., Navarro C. &
Clave P. (2007) Long-term prevalence of
oropharyngeal dysphagia in head and
neck cancer patients: impact on quality
of life. Clinical Nutrition 26, 710–717.
Guigoz Y. & Vellas B.J. (1997) Malnutrition
in the elderly: the Mini Nutritional
Assessment (MNA). Therapeutische
Umschau 54, 345–350.
Haisfield-Wolfe M.E., McGuire D.B.,
Soeken K., Geiger-Brown J. & De Forge
B.R. (2009) Prevalence and correlates
of depression among patients with head
and neck cancer: a systematic review of
implications for research. Oncology
Nursing Forum 36, E107–E125.
Health Promotion Administration (2013)
Health Statistics-Cancer Incidence Sta-
tistics, 2010. Available at: http://www
.hpa.gov.tw/BHPNet/Web/Stat/
Statistics.aspx
Howren M.B., Christensen A.J., Karnell
L.H. & Funk G.F. (2010) Health-related
quality of life in head and neck cancer
survivors: impact of pretreatment depres-
sive symptoms. Health Psychology 29,
65–71.
Jager-Wittenaar H., Dijkstra P.U., Vissink
A., van Oort R.P., van der Laan B.F. &
Roodenburg J.L. (2011) Malnutrition in
cancer–prevalence and relationship with
oral symptoms: an explorative study.
Supportive Care in Cancer 19, 1675–
1683.
Jeyakumar A., Brickman T.M. & Doerr T.
(2006) Review of nasopharyngeal carci-
noma. Ear, Nose, and Throat Journal 85,
168–170, 172–173, 184.
Kamstra J.I., Jager-Wittenaar H., Dijkstra
P.U., Huisman P.M., van Oort R.P., van
der Laan B.F. & Roodenburg J.L. (2011)
Oral symptoms and functional outcome
related to oral and oropharyngeal cancer.
Supportive Care in Cancer 19, 1327–
1333.
Karnofsky D.A., Abelman W.H., Craver L.F.
& Burchenal J.H. (1948) The use of the
nitrogen mustards in the palliative treat-
ment of carcinoma. Cancer 1, 634–656.
Kim S.J., Rha S.Y., Song S.K., Namkoong K.,
Chung H.C., Yoon S.H., Kim G.M. &
Kim K.R. (2011) Prevalence and associ-
ated factors of psychological distress
among Korean cancer patients. General
Hospital Psychiatry 33, 246–252.
Kiyomoto D. (2007) Head and neck
cancer patients treated with chemo-
radiotherapy require individualized
oncology nutrition. Journal of the Ameri-
can Dietetic Association 107, 412–415.
Lai Y.H. (1998) Symptom distress and home
care needs in patients receiving chemo-
therapy in an outpatient setting. Journal
of Nursing Research (Taiwan) 6, 279–
289.
Larsson M., Hedelin B., Johansson I. &
Athlin E. (2005) Eating problems and
weight loss for patients with head and
neck cancer: a chart review from diagno-
sis until one year after treatment. Cancer
Nursing 28, 425–435.
Logemann J.A., Pauloski B.R., Rademaker
A.W., Lazarus C.L., Mittal B., Gaziano J.,
Stachowiak L., MacCracken E. &
Newman L.A. (2003) Xerostomia:
12-month changes in saliva production
and its relationship to perception and
performance of swallow function, oral
intake, and diet after chemoradiation.
Head and Neck 25, 432–437.
Marucci L., Marzi S., Sperduti I.,
Giovinazzo G., Pinnaro P., Benassi M. &
Strigari L. (2012) Influence of intensity-
modulated radiation therapy technique
on xerostomia and related quality of
life in patients treated with intensity-
modulated radiation therapy for
nasopharyngeal cancer. Head and Neck
34, 328–335.
National Cancer Insititute (2013) About
Cancer Survivorship Research: Survivor-
ship Definitions. Available at: http://
dccps.nci.nih.gov/ocs/definitions.html
National Comprehensive Cancer Network
(2012) National Comprehensive Cancer
Network Guidelines. Head and Neck
Cancers V1. Available at: http://www
.nccn.org
Oates J.E., Clark J.R., Read J., Reeves N.,
Gao K., Jackson M., Boyer M. & O’Brien
C.J. (2007) Prospective evaluation of
quality of life and nutrition before and
after treatment for nasopharyngeal carci-
noma. Archives of Otolaryngology–Head
and Neck Surgery 133, 533–540.
Peng G., Wang T., Yang K.Y., Zhang S.,
Zhang T., Li Q., Han J. & Wu G. (2012) A
prospective, randomized study compar-
ing outcomes and toxicities of intensity-
modulated radiotherapy vs. conventional
two-dimensional radiotherapy for the

treatment of nasopharyngeal carcinoma.
Radiotherapy and Oncology 104, 286–
293.
Pignon J.P., Bourhis J., Domenge C. &
Designe L. (2000) Chemotherapy added to
locoregional treatment for head and neck
squamous-cell carcinoma: three meta-
analyses of updated individual data.
MACH-NC Collaborative Group. Meta-
Analysis of Chemotherapy on Head and
Neck Cancer. Lancet 355, 949–955.
Qi M., Guangyuan H., Guoxian L., Hong
Q., Qiang F. & Guoqing H. (2011) A
prospective study on therapeutic gain
by concurrent chemoradiotherapy for
stage II-IV a nasopharyngeal carcinoma.
Journal of Huazhong University of
Science and Technology 31, 58–61.
Rao T.S., Asha M.R., Ramesh B.N. & Rao
K.S. (2008) Understanding nutrition,
depression and mental illnesses. Indian
Journal of Psychiatry 50, 77–82.
Rogers S.N., Johnson I.A. & Lowe D. (2009)
Xerostomia after treatment for oral and
oropharyngeal cancer using the Univer-
sity of Washington saliva domain and a
xerostomia-related quality-of-life scale.
International Journal of Radiation
Oncology, Biology, Physics 77, 16–23.
Rosenthal D.I., Mendoza T.R., Chambers
M.S., Burkett V.S., Garden A.S., Hessell
A.C., Lewin J.S., Ang K.K., Kies M.S.,
Gning I., Wang X.S. & Cleeland C.S.
(2008) The M. D. Anderson symptom
inventory-head and neck module, a
© 2014 John Wiley & Sons Ltd
Nutrition, trismus and dry mouth in nasopharyngeal carcinoma patients
patient-reported outcome instrument,
accurately predicts the severity of
radiation-induced mucositis. Interna-
tional Journal of Radiation Oncology,
Biology, Physics 72, 1355–1361.
Stegenga B., de Bont L.G., de Leeuw R. &
Boering G. (1993) Assessment of man-
dibular function impairment associated
with temporomandibular joint osteoar-
throsis and internal derangement.
Journal of Orofacial Pain 7, 183–195.
Su S.F., Han F., Zhao C., Chen C.Y., Xiao
W.W., Li J.X. & Lu T.X. (2012) Long-term
outcomes of early-stage nasopharyn-
geal carcinoma patients treated with
intensity-modulated radiotherapy alone.
International Journal of Radiation
Oncology, Biology, Physics 82, 327–
333.
Tsai A.C., Chang T.L., Chen J.T. & Yang
T.W. (2009) Population-specific modifica-
tions of the short-form Mini Nutritional
Assessment and Malnutrition Universal
Screening Tool for elderly Taiwanese.
International Journal of Nursing Studies
46, 1431–1438.
Tsai A.C., Yang S.F. & Wang J.Y. (2010)
Validation of population-specific Mini-
Nutritional Assessment with its long-
term mortality-predicting ability: results
of a population-based longitudinal 4-year
study in Taiwan. British Journal of Nutri-
tion 104, 93–99.
Tsai L.Y., Li I.F., Lai Y.H., Liu C.P., Chang
T.Y. & Tu C.T. (2007) Fatigue and its
associated factors in hospice cancer
patients in Taiwan. Cancer Nursing 30,
24–30.
Vissink A., Burlage F.R., Spijkervet F.K.,
Jansma J. & Coppes R.P. (2003a) Preven-
tion and treatment of the consequences
of head and neck radiotherapy. Critical
Reviews in Oral Biology and Medicine
14, 213–225.
Vissink A., Jansma J., Spijkervet F.K.,
Burlage F.R. & Coppes R.P. (2003b) Oral
sequelae of head and neck radiotherapy.
Critical Reviews in Oral Biology and
Medicine 14, 199–212.
Wang Z.H., Yan C., Zhang Z.Y., Zhang
C.P., Hu H.S., Tu W.Y., Kirwan J. &
Mendenhall W.M. (2011) Impact of sali-
vary gland dosimetry on post-IMRT
recovery of saliva output and xerostomia
grade for head-and-neck cancer patients
treated with or without contralateral
submandibular gland sparing: a longitu-
dinal study. International Journal of
Radiation Oncology, Biology, Physics 81,
1479–1487.
Wu V.W., Ying M.T. & Kwong D.L.
(2011) Evaluation of radiation-induced
changes to parotid glands following
conventional radiotherapy in patients
with nasopharygneal carcinoma. British
Journal of Radiology 84, 843–849.
Zigmond A.S. & Snaith R.P. (1983) The
hospital anxiety and depression scale.
Acta Psychiatrica Scandinavica 67,
361–370.
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