Clinical Study
Oncology
DOI: 10.1159/000504449
The Five-Year Survival Rate of Patients with
Nasopharyngeal Carcinoma Based on Tumor
Response after Receiving Neoadjuvant
Chemotherapy, Followed by Chemoradiation,
in Indonesia: A Retrospective Study
Fifi Dwijayanti a Artha Prabawa b Besral b Cita Herawati c
aMaster Study Program of Biostatistics and Population, Faculty of Public Health, Universitas Indonesia, Depok,
Indonesia; bDepartment of Biostatistics and Population Studies, Faculty of Public Health, Universitas Indonesia,
Depok, Indonesia; cDepartment of Ear, Nose, and Throat, National Cancer Center – Dharmais Cancer Hospital,
Jakarta, Indonesia, Depok, Indonesia
Keywords
Survival · Nasopharyngeal carcinoma · Tumor response ·
Neoadjuvant chemotherapy · Chemoradiation
Abstract
Introduction: Nasopharyngeal cancer (NPC) is a common ma-
lignancy in Southeast Asia with a high mortality rate. Previous
studies have shown that the patient survival rate is <80%
worldwide. At the Dharmais Cancer Hospital, NPC is the first
of the top 10 diseases with the highest rate of stage III cancer
progression. Objective: This study aims to determine the
5-year survival rate of patients with NPC based on tumor re-
sponse and their prognostic factors after receiving neoadju-
vant chemotherapy, followed by chemoradiation. Methods:
The records of 261 patients between January 2009 and De-
cember 2013 were retrospectively analyzed. All patients with
NPC who received neoadjuvant chemotherapy, followed by
chemoradiation, at the Dharmais Cancer Hospital from 2009
to 2013 were identified. Patients with metastasis were exclud-
ed. The primary endpoint of this study was overall survival,
which was defined as the time from the date of treatment to
the date of death. The survival curve was analyzed using the
© 2020 S. Karger AG, Basel
E-Mail karger@karger.com
www.karger.com/ocl
Received: October 16, 2019
Accepted: October 20, 2019
Published online: January 27, 2020
Kaplan-Meier method. The Cox proportional hazard model
was used for the multivariate analysis of prognostic factors.
Results: The tumor response rates for patients with complete
response (CR), partial response (PR), and progressive disease
(PD) were 33.7, 45.2, and 21.2%, respectively. The 5-year over-
all survival rate was 38.6%. The 5-year survival rates based on
tumor response among CR, PR, and PD patients were 71.0,
30.4, and 10.6%, respectively. The significant independent
prognostic factors were tumor response, educational back-
ground, job, alcohol consumption, clinical stage, and prompt
treatment. Conclusion: The survival probability of patients
with NPC receiving neoadjuvant chemotherapy, followed by
chemoradiation, was higher in the CR group than in the PR
and PD groups. This confirms that early detection can improve
the patient’s survival. Long-term follow-up is required to de-
termine the factors influencing tumor response in NPC.
© 2020 S. Karger AG, Basel
Introduction
Cancer is the second leading cause of death globally
and was responsible for an estimated 9.6 million deaths
in 2018. Globally, about 1 in 6 deaths is due to cancer. Ap-
193.51.85.197 - 1/30/2020 4:41:42 PM
Prof. Artha Prabawa
Department of Biostatistics and Population Studies, Faculty of Public Health
Universitas Indonesia, Building A, 2nd Floor Kampus UI
Prof dr Sujudi street, Depok 16424 (Indonesia)
Université de Paris
Downloaded by:
E-Mail artha @ ui.ac.id
 1,514 patients newly diagnosed with NPC
in January 2009–December 2013
348 patients performed anatomical
pathology examination at Dharmais
261 patients were included in this study
Fig. 1. Flowchart of the exclusion steps in
this study.
proximately 70% of deaths from cancer occur in low- and
middle-income countries. Cancer is a burden for every
country in the world [1]. Nasopharyngeal carcinoma
(NPC) is different from other head and neck cancers be-
cause its distribution is influenced by geography, and it is
associated with the Epstein-Barr virus [2]. Based on GLO-
BOCAN 2018, there were 129,079 new cases of NPC and
72,987 death [3, 4]. Globally, Southeast Asian countries
constitute 67% of the cancer burden [5].
Epidemiologically, NPC has a specific etiology because
it is influenced by geography and race, i.e., genetic, social,
and environmental factors [6]. Indonesia has a popula-
tion of 225 million people, with an estimated total inci-
dence of 6.2 cases per 100,000 people or about 12,000 new
cases of NPC per year [7]. NPC mostly occurs during the
productive age (40–60 years) and in children. It is more
common in males than in females (3:1). Demographers
often describe the changing age structure in terms of
changing dependency ratios [8].
NPC is the first of the top 10 diseases at the Dharmais
Cancer Hospital, with the highest rates in stages III and
IV. The treatment of NPC includes radiation, chemother-
apy, and a combination of both and is supported by symp-
tomatic therapy according to symptoms presented by the
patients [9]. A study carried out in China revealed that the
largest proportion of tumor response was complete re-
sponse (CR), with a survival rate of 75.5% [10]. In con-
trast, another study by Feryel et al. [11] (2018) revealed
that the largest proportion of tumor response was partial
response (PR), with a survival rate of 54.2%. Peng et al.
[12] (2016) reported the proportion of CR, PR, and pro-
gressive disease (PD) tumor responses to be 25.3, 65.7,
and 9.0%, while the survival rates were 90.0, 79.0, and
58.2%, respectively.
2 Oncology
DOI: 10.1159/000504449
- 464 pathological anatomy data not available
- 340 had metastasis
- 312 medical records not available
- 50 primary diagnosis not NPC after renew
staging
- 30 patients receiving chemotherapy only
- 57 patients receiving radiation only
Only a few studies have examined survival of NPC pa-
tients based on tumor response. Tumor response is an
indicator of treatment effectiveness and patient prognos-
tic factors. There is a difference between the proportion
of tumor responses and the survival rate. Therefore, we
aimed to investigate the 5-year survival rate of NPC pa-
tients based on tumor response of patients receiving neo-
adjuvant chemotherapy, followed by chemoradiation, at
the Dharmais Cancer Hospital.
Materials and Methods
This research is a retrospective cohort study. Incident cases of
NPC were obtained from the Dharmais Cancer Hospital registries.
The clinical stage was determined based on the seventh edition of
the American Joint Committee staging system. Patients with ad-
vanced stages were excluded. All ages were included, including
children. The eligibility criteria were (1) patients that received neo-
adjuvant chemotherapy, followed by chemoradiation; (2) avail-
ability of anatomical pathology results or other supporting results
in medical records; and (3) a complete integrated record and med-
ical history of the patient. Patients with metastasis were excluded.
A total of 1,514 NPC patients were identified between January
2009 and December 2013. We screened the data in two steps. In a
first step, 1,166 of 1,514 patients were excluded (464 pathological
anatomy data were not available, 340 patients had metastases, 312
medical records were not available, and 50 primary diagnosis not
NPC after renew staging). In a second step, 87 patients were ex-
cluded (30 patients receiving chemotherapy and 57 patients receiv-
ing radiotherapy only). 261 patients were included in this study
(Fig. 1). The definition of an event was a patient died because of
NPC, and that of censored was a patient was alive but lost to fol-
low-up in this study.
The data collected were patient demographics, lifestyle, clinical
stage, long-term illness complaint, and tumor response. The de-
mographics of the patients included age, educational background,
job, and gender. The age data were divided into two groups – those
<45 years of age and those ≥45 years. The educational background
193.51.85.197 - 1/30/2020 4:41:42 PM
Dwijayanti/Prabawa/Besral/Herawati
Université de Paris
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of the patients was divided into three groups – high education
(those who graduated from college), middle education (those who
graduated from senior high school), and low education (those who
graduated from elementary and junior high school or did not go
to school).
The duration of treatment of patients with NPC receiving neo-
adjuvant chemotherapy, followed by chemoradiation, was approx-
imately 6 months. Neoadjuvant chemotherapy was done thrice
weekly in 3–4 cycles. Chemoradiation was done weekly, up to 30–
40 times every day. After 7–14 days, an evaluation was carried out
to determine tumor response. Treatment was said to be on time if
completed in <6 months.
Statistical Analysis
The primary endpoint of this study was overall survival (OS),
which was defined as the time from the date of treatment start to
the date of death. The cut-off for patients who survived was defined
as the time of the last visit. After completion of the treatment, pa-
tients were followed up every 3 months in the first 5 years after
neoadjuvant chemotherapy and every 6 months thereafter until
death. Magnetic resonance imaging (MRI) scans with the contrast
of head and neck, computed tomography (CT) scans with contrast,
nasopharyngoscopy, abdominal sonography, and bone scan mea-
surement were routinely performed or upon clinical indication of
tumor response. Positron emission tomography--CT was consid-
ered if necessary. All the results were identified in the medical re-
cords.
Prognostic factors for the NPC patients were determined by
analyzing the relationship between patient survival and the follow-
ing: age, educational background, occupation, gender, smoking,
alcohol consumption, cancer stage, complaints of old disease, and
immediate care. Statistical analysis was performed using Stata. The
survival curve was analyzed using the Kaplan-Meier method. The
Cox proportional hazard model was used for multivariate analysis
of prognostic factors. All analyses were two-sided, and the signifi-
cance level was set at p < 0.05.
Results
A total of 1,514 newly diagnosed cases of NPC were
treated at the Dharmais Cancer Hospital between January
2009 and December 2013. Anatomical pathology exami-
nation was performed on 348 patients. Finally, 261 pa-
tients were included in this study. The flowchart of exclu-
sion steps is shown in Figure 1. The follow-up time was
44 months (range 1–60 months). 117 patients died during
follow-up. The 5-year OS was 38.6%.
Among the 261 patients, 88 (33.7%) achieved CR, 118
(45.2%) achieved PR, and 55 (21.1%) had PD. The CR and
PR proportions of the 5-year OS based on tumor response
of patients receiving neoadjuvant chemotherapy, fol-
lowed by chemoradiation, were 71.0 and 30.4%, respec-
tively. The PD proportion of the 5-year OS was 10.6%.
Cox regression showed that these factors were signifi-
cantly associated with the survival of the patients.
Survival Rate of Nasopharyngeal
Carcinoma
The results showed that the highest proportion of NPC
patients were males, aged ≥45 years, have middle educa-
tion, and were unemployed. Risk factors for NPC patients
are tumor response, smoking, alcohol consumption, clin-
ical stage, long-term illness complain, and prompt treat-
ment. Risk factors that we suspect have an influence on
NPC are tumor response, smoking, clinical stage, and
prompt treatment (Table 1).
In the CR group, 81 out of 88 patients were still alive
with a probability of 92.1% after the first year. After the
second and third years, the probability decreased to 86.9
and 82.3%, respectively. The 5-year survival probability
of NPC patients in the CR group was 71.0%. In the PR
group, 84 out of 118 respondents were still alive with a
probability of 70.3% after the first year. This shows that
34 patients died during 1 year of treatment. In the second
year, the probability decreased to 56.5%. The 5-year sur-
vival probability of NPC patients in the PR group was
30.4%. In the PD group, 16 out of 55 people were still alive
with a probability of 31.3% after the first year. This im-
plies that 39 patients died during 1 year of treatment. The
5-year survival probability of patients with NPC in the PD
group is 10.6%, and our patients only survived for 3 years
(Table 2).
The multivariate analysis confirms hazard ratios (HR)
to determine the effect of risk factors. Multivariate analy-
sis showed that the significant prognostic factors for the
survival of NPC patients were tumor response (PR group,
HR = 2.49, p = 0.001; PD group, HR = 4.75, p < 0.001),
educational background (middle education group, HR =
1.81, p = 0.047; low education group, HR = 1.82, p =
0.090), and prompt treatment (HR = 64.57, p < 0.001).
The confounder variables were job (HR = 0,72, p = 0.161),
alcohol consumption (HR = 0.47, p = 0.118), and clinical
stage (HR = 1.28, p = 0.247) (Table 3). OS rates based on
tumor response are shown in Figure 2. There is a clear
trend of differences in survival between the groups of tu-
mor response (Fig. 2). The probability of survival of NPC
patients is higher in the CR group than in the PR and PD
groups.
Discussion/Conclusion
Tumor response predictions are very important for
planning and modifying treatment. Tumor response was
approved using MRI scans after completing the evalua-
tion based on the Response Evaluation Criteria on Solid
Tumors [13]. CR after induction chemotherapy followed
by chemoradiation is associated with better local control
193.51.85.197 - 1/30/2020 4:41:42 PM
Oncology 3
DOI: 10.1159/000504449
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Table 1. Patient characteristics, demography, and risk factors Table 2. Survival of nasopharyngeal carcinoma patients based on
tumor response
Characteristics Patients,
n (%) Tumor Year Risk Cumulative 95% CI
response population survival, %
Age groups
<45 years 124 (47.5) Complete First 81 92.1 80.4–96.1
≥45 years 137 (52.5) response Second 59 86.9 77.5–92.5
Educational background Third 29 82.3 70.7–89.7
Higher education (college graduate) 41 (15.7) Fourth 14 71.0 53.8–82.8
Middle education (senior high school) 131 (50.2) Fifth 9 71.0 53.8–82.8
Low education (elementary and junior
high school) 89 (34.1) Partial First 84 70.3 61.1–77.7
Job reponse Second 34 56.5 46.4–65.4
Unemployed 146 (55.9) Third 15 44.4 32.0–55.9
Employed 115 (44.1) Fourth 7 30.4 16.0–46.1
Gender Fifth 2 30.4 16.0–46.1
Female 73 (27.9) Progressive First 16 31.3 19.5–43.8
Male 188 (72.1) disease Second 8 17.3 8.1–30.4
Tumor response   Third 4 10.6 3.2–23.3
Complete response 88 (33.7) Fourth 0 0 0
Partial response 118 (45.2) Fifth 0 0 0
Progressive disease 55 (21.1)
Smoking
No 128 (49.1)
Yes 133 (50.9)
Alcohol consumption Table 3. The final model of the Cox regression for the 5-year sur-
No 250 (95.8) vival rate of nasopharyngeal carcinoma patients
Yes 11 (4.2)
Clinical stage Variable HR 95% CI p value
Stage III 91 (34.9)
Stage IVA 170 (65.1) Tumor response
Long-term illness complaint CR Reference Reference
<6 months 76 (29.1) PR 2.49 1.36–4.53 0.001**
≥6 months 185 (70.9) PD 4.75 2.49–0.06 <0.001**
Prompt treatment
Education
Yes 125 (47.9)
Middle education 1.81 1.01–3.25 0.047*
No 136 (51.1)
Low education 1.82 0.91–3.64 0.090
Job 0.72 0.46–1.14 0.161
Alcohol consumption 0.47 0.18–1.21 0.118
Clinical stage 1.28 0.84–1.96 0.247
than radiotherapy alone (85 vs 73%). The OS after induc- Prompt treatment 64.57 14.90–279.77 <0.001**
tion chemotherapy was 38 months in the CR group and T-cov prompt treatment 0.91 0.86–0.97 0.002**
30 months in the PR group (p > 0.05) [11]. The results of
HR, hazard ratio; * significance p < 0.05; ** p < 0.01.
the meta-analysis confirmed that patients receiving com-
bined modalities (neoadjuvant, concurrent, or adjuvant
chemotherapy) have the absolute benefit of event-free
survival and OS [14].
Unsatisfactory tumor response, such as PD, can pre- Richard et al. [19] (2016) reported in their study that
dict a poor prognosis for patients at an advanced stage of NPC death rates in children and adults were higher in ar-
NPC (locoregional relapse-free survival, progression-free eas with lower median household income and in areas
survival) [15, 16]. Other studies have concluded that with lower educational achievement. Higher education
overall tumor response after induction chemotherapy is contributed to the survival of the patients. This shows
an independent prognostic factor for disease-free surviv- that the level of education affects the knowledge, behav-
al, OS, and survival free of locoregional recurrences [12– ior, and ability of patients to care for themselves and deal
18]. with illnesses [20].
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4 Oncology Dwijayanti/Prabawa/Besral/Herawati
DOI: 10.1159/000504449
Université de Paris
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1.00
0.75
0.50
0.25
0
Fig. 2. Overall survival rates based on tu- 0 20
mor response. CR, complete response; PR,
partial response; PD, progressive disease.
Nutrition in cancer patients also greatly affects the
body’s response to the treatment. An unhealthy lifestyle
can affect the survival of cancer patients. Patients with poor
nutrition cannot survive the treatment, especially chemo-
therapy [21, 22]. Patients’ history, especially smoking, al-
cohol and tobacco consumption, contains main cancer risk
factors. They are associated with increased oxidative stress
and decreased antioxidant serum at the micronutrient lev-
el [23]. Sanda et al. [24] (2016) showed that nutritional
status has an important impact on the response rate, treat-
ment tolerance, performance status, and quality of life.
The 5-year survival rate of NPC patients at stage III
was 51.5%, whereas at stage IVA it was 32.4%. The inva-
sion of a carcinoma can be attributed to the speed of
growth and the relationship between cells in NPC. The
greater the ability of cancer cells to invade, the farther the
invasion location, and the higher the stage. This makes
the clinical stage an important parameter in determining
the severity or prognosis, and it is used as the main basis
for treatment [25].
The NPC patients at the Dharmais Cancer Hospital
were dominated by patients at stage IVA and stage III. Al-
most all of our NPC patients came to the hospital at an ad-
vanced stage. Ensuring patients are treated at an early age
was very difficult because the location of the NPC is hidden
such that the patient only feels it or complains of symptoms
when the tumor has spread [26]. The 5-year survival after
prompt treatment is higher than after late treatment. Until
now, the modalities commonly used in the follow-up of
patients with NPC included clinical examination and dis-
ease staging studies [27]. Uncertain diagnosis can cause
delayed treatment, which can reduce the life expectancy of
patients with recurrent NPC lesions [28].
The detection of NPC at early stages is often difficult be-
cause the symptoms are not specific. Many patients are di-
Survival Rate of Nasopharyngeal
Carcinoma
Color version available online
Tumor response = CR
Tumor response = PR
Tumor response = PD
40 60
Analysis time, months
agnosed at an advanced stage because the initial symptoms
do not cause discomfort. This results in a lack of motivation
to seek medical treatment. Head and neck cancers, espe-
cially NPC, are often diagnosed when they have reached an
advanced stage. Delays in diagnosis and treatment make
prognosis much worse. Another reason for delayed treat-
ment may be a lack of access to health-care facilities [29].
The 5-year survival of NPC patients receiving neoad-
juvant chemotherapy, followed by chemoradiation, was
38.6%. The proportion of CR tumor response in patients
who survived is higher than those of PR and PD. The sig-
nificant independent prognostic factors are tumor re-
sponse, educational backgrounds, job, alcohol consump-
tion, clinical stage, and prompt treatment. We suggest
working closely with hospitals of type B, C, and other
health-care providers to introduce early detection of NPC
through seminars or counseling of general practitioners
and the public. Our findings showed that early detection
could improve patients’ survival. Further prospective
randomized studies are required to uphold the results of
this study.
Acknowledgement
We kindly thank Mr. Aris for helping with the medical records
and the Dharmais Cancer Hospital for providing access to the
medical records used in this research.
Statement of Ethics
This study was approved by the Ethical Committee of the Fac-
ulty of Public Health at Universitas Indonesia (approval No.: 018/
UN2.F10/PPM.00.02/2019) and the Research Ethics Committee
from the Dharmais Cancer Hospital (approval No.: 016/KEPK/
II/2019).
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Oncology 5
DOI: 10.1159/000504449
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 Disclosure Statement
The authors have no conflicts of interest to declare.
Funding Sources
This study was sponsored by Universitas Indonesia through
Hibah Publikasi Internasional Terindeks (Hibah PITTA B; No.:
NKB-0595/UN2.R3.1/HKP.05.00/2019).
Author Contributions
Fifi Dwijayanti (FD), Artha Prabawa (AP), Besral (BS), Cita
Herawati (CH):
FD and CH conceived the presented idea. FD developed the
theory and performed the computations. AP verified the content
based on academic writing, and BS verified the analytical methods.
AP encouraged FD to investigate (a specific aspect) and supervised
the findings of this work. BS suggested to FD to use multivariate
analysis. All authors discussed the results and contributed to the
final manuscript.
FD accessed the data in the medical records at the hospital, and
CH verified the data especially patient’s diagnosis. FD and CH
conceived the original idea. AP and BS supervised the project. FD
wrote the manuscript with support from AP and BS. FD developed
the theoretical formalism with support from AP and CH. BS per-
formed the analytic calculations and interpretation. FD, AP, and
BS contributed to the final version of the manuscript. CH super-
vised the project. All authors provided critical feedback and helped
shape the research, analysis, and manuscript.
FD, AP and CH designed the model. FD and BS did the com-
putational framework and analyzed the data. FD, BS, and AP per-
formed the calculations. FD wrote the manuscript with input from
all other authors. CH and FD conceived the study and were in
charge of overall direction and planning in getting the data. FD
devised the project, the main conceptual ideas, and proof outline.
FD, AP, and BS performed the measurements, AP and CH were
involved in planning and supervised the work, FD and BS pro-
cessed the data, performed the analysis, drafted the manuscript,
and designed the figures. AP, BS, and CH aided in interpreting the
results and worked on the manuscript. All authors discussed the
results and commented on the manuscript. FD and CH contrib-
uted to the design and implementation of the research. AP and BS
contributed to the analysis of the results and to the writing of the
manuscript.

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