Acta Otorrinolaringol Esp.

2018;69(6):339---344

www.elsevier.es/otorrino

ORIGINAL ARTICLE

Salvage Surgery in the Treatment of Local Recurrences

of Nasopharyngeal Carcinomas夽
María Cecilia Salom, Fernando López, Esteban Pacheco, Gabriela Muñoz,
Patricia García-Cabo, Laura Fernández, Vanessa Suárez, José Luis Llorente∗

Unidad de Base de Cráneo, Servicio de Otorrinolaringología, Hospital Universitario Central de Asturias, ISPA, IUOPA, Universidad
de Oviedo, CIBERONC, Oviedo (Asturias), Spain

Received 26 July 2017; accepted 21 November 2017

KEYWORDS Abstract
Nasopharynx; Introduction and Objectives: Chemoradiotherapy is the treatment of choice for nasopharyngeal
Endoscope; carcinoma. Local recurrences are one of the leading causes of death in these patients, and
Nasopharynx surgical salvage the treatment of choice. Our goal was to evaluate and compare the results of
carcinoma; salvage surgery in the treatment of local recurrence of nasopharyngeal carcinomas comparing
Endonasal endoscopic to open approaches.
nasopharyngectomy Methods: Twenty patients with local recurrence of nasopharyngeal carcinomas underwent
surgery: 12 patients underwent open surgery and 8 endoscopic endonasal transpterygoid
nasopharyngectomy. One patient was classified as rT1, three as rT2, two as rT3, and six as
rT4 in the group of open approaches; in the endoscopic series, two patients were rT1, five rT2
and one rT3.
Results: In 3 patients (25%) operated by an open approach (one rT4, one rT3 and one rT2) a
complete gross resection was not achieved. Gross total resection was achieved in patients oper-
ated by endoscopic surgery. The complication rate in the group operated by an open approach
was 92% (five minor complications, five moderate complications, and one serious complication)
and in the group that underwent endoscopic surgery all patients had some complication (seven
had minor complications and one patient developed a severe complication). Survival at 3 and 5
years was 53% and 42% with the open approach and 100% and 50% with the endoscopic approach,
respectively.
Conclusions: Endoscopic approaches decrease the morbidity associated with open approaches
and allow for favourable oncological control.
© 2018 Sociedad Española de Otorrinolaringologı́a y Cirugı́a de Cabeza y Cuello. Published by
Elsevier España, S.L.U. All rights reserved.

夽 Please cite this article as: Salom MC, López F, Pacheco E, Muñoz G, García-Cabo P, Fernández L, et al. Cirugía de rescate en las recidivas

locales del carcinoma de nasofaringe. Acta Otorrinolaringol Esp. 2018;69:339---344.

∗ Corresponding author.

E-mail address: llorentependas@telefonica.net (J.L. Llorente).

2173-5735/© 2018 Sociedad Española de Otorrinolaringologı́a y Cirugı́a de Cabeza y Cuello. Published by Elsevier España, S.L.U. All rights
reserved.
340 M.C. Salom et al.

PALABRAS CLAVE Cirugía de rescate en las recidivas locales del carcinoma de nasofaringe
Nasofaringe;
Resumen
Endoscopia;
Introducción y Objetivos: La quimiorradioterapia es el tratamiento de elección del carcinoma
Carcinoma de
de nasofaringe. Las recurrencias locales son una de las principales causas de mortalidad en
nasofaringe;
estos pacientes: el rescate quirúrgico o la reirradiación son el tratamiento de elección, según
Nasofaringectomía
la disponibilidad. El objetivo fue evaluar y comparar los resultados de la cirugía de rescate
endoscópica
en el tratamiento de las recidivas locales de los carcinomas nasofaríngeos mediante abordajes
abiertos vs. endoscópicos.
Métodos: Veinte pacientes con recidivas locales de carcinomas nasofaríngeos fueron inter-
venidos quirúrgicamente: 12 pacientes fueron intervenidos mediante cirugía abierta y 8
mediante un abordaje endoscópico endonasal transpterigoideo. Un paciente fue estadiado como
rT1; 3 como rT2; 2 como rT3 y 6 como rT4 en el grupo de abordajes abiertos; en la serie
endoscópica, 2 pacientes fueron rT1, 5 fueron rT2 y uno fue rT3.
Resultados: En 3 de los pacientes (25%) intervenidos mediante cirugía abierta (un rT4, un rT3 y
un rT2) no se logró una resección macroscópica completa). En el grupo endoscópico la resección
fue completa en todos los pacientes. La tasa de complicaciones en el grupo intervenido medi-
ante abordajes abiertos fue del 92% (5 complicaciones leves, 5 complicaciones moderadas y una
complicación grave) y en el grupo intervenido mediante endoscopia fue del 100% (7 sufrieron
complicaciones leves y un paciente una complicación grave). La supervivencia a los 3 y 5 años
fue del 53 y del 42% en el abordaje abierto y del 100 y del 75% en el abordaje endoscópico,
respectivamente.
Conclusiones: Los abordajes endoscópicos disminuyen la morbilidad asociada a los abordajes
abiertos y permiten obtener un control oncológico favorable.
© 2018 Sociedad Española de Otorrinolaringologı́a y Cirugı́a de Cabeza y Cuello. Publicado por
Elsevier España, S.L.U. Todos los derechos reservados.

Introduction Several surgical approaches have been described for

Nasopharyngeal carcinoma (NC) is a radiosensitive tumour
and radiotherapy (RT) is the first treatment option.1 In ini-
tial stages (I and II) the NC is treated with RT while in
advanced stages (III and IV) it is treated with concomitant
chemoradiotherapy.2,3 With advances in RT techniques, such
as intensity-modulated RT (IMRT) and intensity-modulated
volumetric arc therapy and the administration of concomit-
tant chemoradiotherapy, local control rates at five years are
between 76% and 91%.3,4 However, between 20% and 50% of
patients develop local recurrences during the 5 years fol-
lowing the appearance of the disease, and this is a major
cause of morbidity and mortality.5
When a local recurrence occurs, salvage treatment must
be intensive, as patients who receive salvage treatment
have a considerably better overall survival rate than those
who do not. Treatment of NC recurrences is still complex
and early detection of recurrence is vital for any sal-
vage therapy to be effective.5 Available therapeutic options
include re-irradiation, chemotherapy and surgery. The role
of chemotherapy is principally reserved for palliative care
for those patients who are not suitable candidates for re-
irradiation or surgery.6 Re-irradiation achieves low local
control rates7 and complications are frequent and serious.8
As a result, surgery presents a reasonable option when recur-
rence may be resected. Local control rates are satisfactory
and morbidity is lower to high dose re-irradiation.9
this type of tumour,10 but no consensus has been reached
regarding which is the best technique for obtaining com-
plete resection of the tumour with the lowest rate of
morbidity. The optimum approach will depend on the
size and location of the tumour. Standard approaches
used have been anterior external (transpalatal, transmax-
illary, transmandibular, facial translocation) and lateral
(subtemporal-periauricular).9,11 These approaches result in
significant morbidity, as they interfere with a previously irra-
diated region. An attempt has been made to reduce the
morbidity rates associated with open surgery by the progres-
sive use of minimally invasive endoscopic approaches.12,13
The aim of this study is to present our experience in
the surgical treatment of local recurrences of NC, mainly
focussing on the type of surgical approach used.
Method
The surgical record of the otorhinolaryngology department
of our hospital was reviewed from 1994 until 2014 and data
was collected from the medical histories relating to patients
with a diagnosis of local recurrence of NC.
Data collection was based on the review of medical histo-
ries, with recording of data on age, gender, prior treatments,
spread and staging of tumour, mean time from treat-
ment of primary tumour to recurrence, surgical approach,
complications and follow-up.
Salvage surgery in the treatment of nasopharyngeal carcinomas
The study population comprised 20 patients who had
undergone surgery. Open surgery was used on the first
12 patients (60%),as has already been described for our
group14 : six patients underwent anterior facial translocation
surgery and six subtemporal-preauricular surgery.6,11 Since
2002, due to the standardisation of extended endoscopic
endonasal approaches for the treatment of these tumours,
the 8 patients (40%) underwent endoscopic endonasal
transpterigoid surgery (Castelnuovo type 3 resection).15
Radiologic studies were performed on all patients prior
to surgery using computerised tomography CT and magnetic
resonance (MR) imaging. Patients also had a chest X-ray, an
abdominal scan, a bone scan in the cases of open surgery14
and CT, MR and positron emission tomography (PET) in the
cases of endoscopic surgery. Only patients with no pres-
ence of distance metastasis were operated on. Statistical
data analysis was performed with the SPSS programme for
Windows version 11.0.
Results
The sample comprised 14 male patients and 6 Female
patients with a mean age at time of intervention of 54
years (range 42---73). In accordance with the histopatho-
logical classification of the World Health Organisation,16 6
patients presented with stage II tumours and the other 14
with stage III tumours. At initial diagnosis, 7 patients pre-
sented with tumours which were classified as T1, 6 as T2,
3 as T3 and 4 asT4, in accordance with the 7th edition of
the TNM system of the International Union against Cancer17
(Table 1).
For treatment of the primary tumour and cervical nodes
all patients received conformal chemotherapy and RT (3D-
CRT). The mean dose applied on the nasopharynx was
65.5 Gy (range 50---72) and the mean dose received on the
cervical nodes was 44 Gy (range 32---60).
Table 1 Clinical Characteristics of the Patients.
Gender
Age
Histology
(OMS)
rT
Surgical time in minutes
Intraoperative complications
Complications
Hospital stay (days)
Mean follow-up (years)
3 and 5 years survival in %
Local relapse post treatment in months (mean)
341
Two months after finalisation of treatment assessment
was made of the response through a nasofibroscopic exam-
ination and a cervical exploration, together with the
performing of CT or MR imaging. This same assessment
was performed as follow-up every 3 months for 2 years
then every 6 months for 5 years and annually for 10 years
after that. In our series, after finalising treatment complete
response was obtained in all patients.
Local recurrences presented between 7 and 72 months
after finalisation of treatment with RT (mean: 33 months).
Relapses were diagnosed mainly in advanced stages in the
open surgery series and in early stages in the endoscopic
series: one patient was staged as rT1, 3 as rT2, 2 as rT3 and
6 as rT4 in the open surgery group whereas in the endoscopic
series group 2 patients were staged as rT1, 5 rT2 and one
rT3. On diagnosis of local recurrence, none of the patients
presented with regional or distance recurrences and all of
them had received curative surgery both in the open and
endoscopic series.
In 3 of the 12 patients who underwent open surgery
the surgical margins were microscopically affected by the
tumour (one rT4, one rT3 and one rT2). In a fourth patient
due to the spread of the tumour to the parasellar region
which affected a macroscopically incomplete resection, the
administration of adjuvant chemotherapy and stereotaxic
RT were required. In the endoscopic series, in all patients
(8) free tumour margins were obtained.
In the open surgery approach patient series all patients
presented with some kind of complication: 5 patients pre-
sented with minor complications (trismus, serous otitis,
facial paresthesias, haematomas or dehiscences of surgical
wound) and 5 suffered from complications classed as mod-
erate which led to permanent sequelae or required further
surgery (osteomyelitis, necrosis of the temporal lobe, cere-
brospinal fluid fistule. One patient, classified as rT4, as a
result of the appearance of an osteomyelitis of the malar
bone, developed a fistule between the zygomatic region and
Open surgery approach Endoscopic approach
(1994---2001) 12 patients (2002---2014) 8 patients
Males: 9 Males: 5
Females: 3 Females: 3
55 years of age (42---71) 52 years of age (43---73)
Stage II: 2 Stage II: 2
Stage III: 10 Stage III: 6
rT1: 1 rT1: 2
rT2: 3 rT2: 5
rT3: 2 rT3: 1
rT4: 6
>240 <240
1 0
Minor 5 Minor 7
Moderate 5 Moderate 0
Severe 2 Severe 1
19 5
2 >3
53 and 42 100 and 75
7---72 (33) 7---36 (23)
342
the oral cavity which required the addition of a parascapu-
lar free flap to close it. Another patient, also classified as
rT4, died 18 days following surgery as a result of aspiration
pneumonia, after a massive posterior epistaxis during the
immediate post operative period. In the endoscopic series 8
patients presented with complications: 7 patients presented
a minor complication (serous otitis) whilst one patient (rT1)
presented with an osteomyelitis at the base of the skull
several months after surgery.
Minimum patient follow-up is 3 years. At present 11
patients (55%) are living and disease free; 5 patients under-
went open surgery (42%s) and 6, endoscopic surgery (75%s).
In the group of patients who underwent open surgery 7
patients died (4 rT4, one rT3 and 2 rT2): in 6 this was a result
of the local recurrence of the disease (5) or due to a lymph
node recurrence (1) and in one it occurred during the imme-
diate postoperative period (rT4). None of the endoscopically
intervened patients had any repeated local relapses. How-
ever, 2 patients died, one (rT1) due to radionecrosis and
exposure of the skull base and the other due to aspiration
pneumonia (rT3), related to palatal incompetence.
Overall survival of the patients who underwent open
surgery at 3 and 5 years was 53% and 42%, respectively,
whereas at 3 and 5 years in the case of those who under-
went endoscopic surgery it was 100% and 75% respectively.
In the open surgery patient group those cases where tumour
free surgical margins were achieved (8) presented with a
higher survival rate to those whose margins were affected
(4) (P=.0327), all of whom died.
Discussion
Therapeutic options for NC relapses include surgery and RT.15
Both achieve acceptable outcomes with regards to local con-
trol, especially when recurrences are not very widespread
and there is no major intracranial involvement.18
Re-irradiation of local recurrences achieve a survival rate
at 5 years which oscillates between 8% and 36%, with a signif-
icant correlation between re-irradiation dose and survival.
The best local control rates are obtained with accumulated
doses of radiation of at least 60 Gy.9 The main disadvantage
of RT is its low tolerance to the radiation of the nearby
structures, resulting in frequent late complications being
frequent and varying between 26% and 57% of patients.19,20
Treatment mortality ranges from 2% to 10% and is mainly due
to damage of the central nervous system.21 New radiation
techniques such as IMRT, intensity-modulated volumetric arc
therapy, tomotherapy and proton-therapy has resulted in
Table 2 Open Surgery Series Outcomes.
Number Local control
of cases (%) (5 years)
Fee9 37 67
Vlantis24 79 62.8
King8 31 53
Wei5 60 62
Chang30 38 60 (3 years)
Cabanillas14 12 53
M.C. Salom et al.
high levels of dose in the tumour tissues, preserving adja-
cent healthy tissues, which increases therapeutic efficacy
compared with standard techniques. Several series where
IMRT was used have been show to be an excellent local
control, with survival figures of >90% after one year and
acceptable toxicity levels.2,22 However, these RT modalities
are not always available and in some cases the previous RT
doses rule out the use of new irradiation, survival rates after
5 years are yet to be studied.
In general, patients with local recurrences are considered
not to be candidates for surgery when there is invasion of the
cavernous sinus or internal carotid artery or tumours with
intracerebral invasion. In the remainder of cases, surgery
could be taken into consideration as salvage treatment.
Many approaches have been described for the treatment
of this type of tumour: transmandibular, Fisch infratempo-
ral fossa approach type C, subtemporal-preauricular, facial
translocacion (lateral or anterior), maxillary swing type and
transpalatal.23,24 These open surgery approaches, either in
isolation or combined, target the nasopharynx and skull
base. However, the rate of complications is high, bearing
in mind prior RT. Standardised open surgery approaches
have become more limited however and continue to be
used for large tumours, particularly when the nasal cavities,
the posterior wall of the maxillary sinus, the pterygopala-
tine fossa or the infratemporal fossa are compromised. The
method of choice is facial translocation. Facial transloca-
tion with midface degloving and hemicoronal pre-auricular
incision has enabled the avoidance of sequelae associated
with facial incisions occurring with the standard surgical
approach. After RT osteomyellitis is common or the reab-
sorption of the translocated segment. This is minimised
with the use of a temporal flap or performing pediculated
maxillary osteotomy to the soft tissue of the cheek.25 The
subtemporal pre-auricular approach is used mainly when
the tumour has a limited anterior extension but affects
the infratemporal fossa, towards the floor of the middle
fossa or the parasellar region. This also allows for bilat-
eral access of the cavum. One complication specific to the
subtemporal pre-auricular route is trismus, which presented
in all patients of our series treated with this approach,
although at different stages and was never incapacitating.
We should consider that, due to prior RT, the permeability
of the deep temporal arteries may be affected, and using
the temporal muscle for reconstruction is therefore rejected
(Table 2).
Disease-free survival after 5 years of the patients in
our series who underwent open surgery was 42%, which
is within the range described in the literature (20%---44%).
Survival (%) (5 Complications
years) (%)
52 54
51.9 47
47 ---
49 ---
73 (3 years) ---
42 41.6
Salvage surgery in the treatment of nasopharyngeal carcinomas
Table 3 Endoscopic Series Outcomes.
Patients Staging
Chen16 37 rT1N0M0: 17
rT2aN0M0: 4
rT2bN0M0: 14
rT3N0M0: 2
Ko28 28 rT1N0: 12
rT2aN0: 14
rTaN1: 2
Castelnuovo15 8 rT1: 4
rT2a: 1
rT3: 3
Salom 8 rT1: 2
rT2: 5
rT3: 1
Similarly to other series, stage T was an essential factor of
prognosis.8,12,15,23
Endoscopic surgery for the treatment of recurrences of
NC was introduced at the beginning of 2000 and after, firstly
for the treatment of tumours rT1, rT2 and rT3.26 Endo-
scopic procedures may now be used in most salvage surgery
after local recurrence. Endoscopic approaches enable the
targeting of tumours with a more direct exposure and
with less handling of the neurovascular structures and the
avoidance of osteotomies. Oncological results are similar
to those obtained with standard open surgery methods
and fragmented resection of tumours does not appear to
compromise the oncological outcomes provided that the
resection margins are negative. From the patient’s view-
point, the reduction of time in surgery and hospital stay,
a lower rate of complications and the absence of facial inci-
sion are advantages of endoscopic approaches. With regards
to our series: our average time in surgery was 240 min, mean
hospital stay was 5 days and there were no intraoperative
or postoperative complications.
The performing of endoscopic nasopharyngectomy is a
complex technique due to the proximity of critical neu-
ral and vascular structures, and also to the meninges and
central nervous system.15 However, endoscopic resection
outcomes of these tumours are promising27,28 and the results
of our series are similar to those described by other authors
(Table 3).15,16,28
You et al.29 published a series of 144, in which they com-
pared 72 patients who had undergone endoscopic surgery
and 72 patients with IMRT. They concluded that the endo-
scopic surgery increased overall survival at 5 years (77.1% vs
55.5%; P=.003), increased quality of life (global health status
57.6 vs 29.8; P<.001), reduced post treatment complications
(12.5% vs 65.3%; P<.001) and that procedure costs were low
(2371.71 vs 11 847.80 D ; P<.001). Na’ara et al.27 published
an analysis with a series of 779 patients (rT1---2: 655
(83%), rT3---4:129 (16.67%), 661 (84.4%) with open surgery
approaches and 118 (15.1%) endoscopic approaches. At 5
years, they described an overall survival and a disease-free
survival of 58% and 63.4%. In this study, multivariate analysis
showed that endoscopic surgery offers better outcomes in
T3---rT4 in selected patients and that adjuvant re-irradiation
343
Margins Follow-up Survival
(months)
36 (−) 6---45 84% (2 years)
1 (+)
25 (−) 3---48 rT1: 91% (2 years)
3 (+) rT2a: 39% (2 years)
8 (−) 10---78 No recurrences
8 (−) 12---72 No recurrences
offers an advantage of additional survival over surgery
alone. Other authors have achieved a good local control
rate with endoscopic surgery in the initial stages of rT1
and rT2 tumours, whilst open surgery is preferred in
advanced stages.30 Indication could be cautiously extended
to selected rT3 tumours with limited involvement of the
skull base. rT4 patients generally present with a repeated
local recurrence or die due to metastasis.11 In accordance
with these authors, in our endoscopic series, 7 out of the 8
patients were rT1---T2 and only one was rT3, and we there-
fore agree with the indication for this approach. In extensive
recurrences (rT3 and, above all, rT4), in our experience,
the performing of facial translocation or a subtemporal
pre-auricular13 approach are the ones of choice.
Conclusions
Although open surgery and endoscopic procedures appear
to be equally effective in patients who require surgi-
cal salvage, the advantages of the endoscopic skull base
approaches include shorter hospital stays, have a lower rate
of complications and a better quality of life.
Conflict of Interests
The authors have no conflict of interests to declare relating
to this study. We did not receive any financing.
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