Superselective neck dissection: rationale, indications, and results

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European Archives of Oto-Rhino-Laryngologyand Head & Neck ISSN 0937-4477 Eur Arch OtorhinolaryngolDOI 10.1007/s00405-012-2344-5

Superselective neck dissection: rationale,indications, and results

Carlos Suárez, Juan P. Rodrigo,K. Thomas Robbins, Vinidh Paleri, CarlE. Silver, Alessandra Rinaldo, JesusE. Medina, et al.

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REVIEW ARTICLE

Superselective neck dissection: rationale, indications, and results

Carlos Suarez • Juan P. Rodrigo • K. Thomas Robbins • Vinidh Paleri •

Carl E. Silver • Alessandra Rinaldo • Jesus E. Medina • Marc Hamoir •

Alvaro Sanabria • Vanni Mondin • Robert P. Takes • Alfio Ferlito

Accepted: 19 December 2012

� Springer-Verlag Berlin Heidelberg 2013

Abstract It has been established that an appropriately

indicated selective neck dissection can achieve the same

oncologic results as more extensive dissections. An even

more modified selective neck dissection, termed superse-

lective neck dissection, involves the compartmental

removal of the fibrofatty tissue contents within the defined

boundaries of two or fewer contiguous neck levels. Evi-

dence from retrospective studies suggests that superselec-

tive neck dissection (SSND) is oncologically sound for two

indications: elective treatment of the clinically N0 neck

and salvage treatment of persistent lymph node disease

after chemoradiotherapy. While there is broader support for

the former scenario, evidence that SSND may constitute

optimal treatment in the latter is in conformity with the

trend toward developing surgical techniques that provide

better functional outcomes without compromising efficacy.

Keywords Neck dissection � Selective neck dissection �Superselective neck dissection � Neck metastases �Neck levels

This paper was written by members and invitees of the International

Head and Neck Scientific Group (www.IHNSG.com).

C. Suarez � J. P. Rodrigo

Department of Otolaryngology, Hospital Universitario

Central de Asturias, Oviedo, Spain

C. Suarez � J. P. Rodrigo

Instituto Universitario de Oncologıa del Principado

de Asturias, Oviedo, Spain

K. T. Robbins

Division of Otolaryngology-Head and Neck Surgery, Southern

Illinois University School of Medicine, Springfield, IL, USA

V. Paleri

Department of Otolaryngology-Head and Neck Surgery,

Newcastle upon Tyne Foundation Hospitals NHS Trust,

Newcastle upon Tyne, UK

C. E. Silver

Departments of Surgery and Otolaryngology-Head and Neck

Surgery, Albert Einstein College of Medicine,

Montefiore Medical Center, Bronx, NY, USA

A. Rinaldo � V. Mondin � A. Ferlito (&)

ENT Clinic, University of Udine, Piazzale S. Maria della

Misericordia, 33100 Udine, Italy

e-mail: [email protected]

J. E. Medina

Department of Otorhinolaryngology, The University

of Oklahoma Health Sciences Center, Oklahoma City, OK, USA

M. Hamoir

Department of Head and Neck Surgery, Head and Neck

Oncology Program, St Luc University Hospital and Cancer

Center, Brussels, Belgium

A. Sanabria

Department of Surgery, Universidad de Antioquia-Universidad

de La Sabana, Medellın, Colombia

A. Sanabria

Oncology Unit-Hospital Pablo Tobon Uribe, Medellın,

Colombia

R. P. Takes

Department of Otolaryngology-Head and Neck Surgery,

Radboud University Nijmegen Medical Center, Nijmegen,

The Netherlands

123

Eur Arch Otorhinolaryngol

DOI 10.1007/s00405-012-2344-5

Author's personal copy

http://www.IHNSG.com

Introduction

Cervical lymphadenectomy plays a key role in the man-

agement of head and neck squamous cell carcinoma

(HNSCC), as these tumors frequently metastasize to the

lymph nodes in the neck. Cervical metastasis is an

important prognostic factor. In the past century, various

types of neck dissection were employed for surgical

treatment of the neck [1]. Radical neck dissection (RND)

was considered the standard treatment for neck metastasis

for a long time. During the second half of the 20th century,

modifications of the RND were introduced to minimize

post-operative morbidity, which initially included preser-

vation of nonlymphatic structures and was later followed

by techniques to preserve selected nodal groups. The

functional neck dissection developed by Suarez [2] in

1952, became increasingly accepted during the 1960s and

1970s and eventually became the procedure of choice for

elective surgical treatment of the neck in HNSCC. The

functional neck dissection, subsequently termed ‘‘modified

radical neck dissection (MRND)’’ and later ‘‘MRND type

III,’’ includes the removal of the lymph nodes in levels I

through V while preserving the sternocleidomastoid mus-

cle, internal jugular vein, spinal accessory nerve, and

submandibular salivary gland. Jesse et al. [3] introduced

the concept of preserving selected nodal groups which was

also referred to as a modified neck dissection. Later the

term selective neck dissection (SND) was proposed [4]

which was subsequently defined as a cervical lymphade-

nectomy in which there is preservation of one or more of

the lymph node groups that are routinely removed in the

RND [5]. This more limited dissection, confined only to the

first few node levels at risk for metastasis would, in cases

with clinically negative (N0) necks, but with early meta-

static involvement, produces results comparable with those

obtained by more extensive dissection of the neck.

More recently, surgeons began to employ SND for

clinically positive necks, in selected cases, usually with N1

disease. The selection of lymph node levels removed was

based on the expected pattern of metastases of a certain

primary tumor site. The objective of these selective pro-

cedures was to achieve regional control while reducing the

morbidity of surgical neck treatment.

The terminology for description of SND procedures was

based on the classification system of lymph node levels

published by the American Head and Neck Society [5].

SNDs were categorized according to the levels cleared and

this included supraomohyoid (I, II, III), anterolateral (I, II,

III, and IV), lateral (II, III, and IV), and posterolateral (II, III,

IV, and V). In the 2002 revision [6], it was recommended

that the specific names for different types of SND be

dropped and substituted by naming the levels dissected

in parentheses (i.e., supraomohyoid neck dissection was

changed to SND I–III). Recently, a more specific and

comprehensive nomenclature system has been proposed [7].

There is considerable evidence in the literature that SND

can achieve the same oncologic results as more extensive

dissection [8–14]. This raises the question of whether fur-

ther limitation of the dissection may be oncologically

sound. These more limited procedures have been referred

to as superselective neck dissection (SSND) [15], and may

be expected to further reduce operative morbidity [14, 16],

without compromising oncologic outcomes.

The aim of this review is to present evidence supporting

the application of SSND in two specific settings: primary

treatment in the clinically node negative neck and treatment

of persistent neck disease after initial chemoradiotherapy.

Studies supporting rationale and indications

for superselective neck dissection

The clinically negative neck

Standard SND usually involves removal of three node lev-

els. SSND has been defined as the complete removal of all

fibrofatty tissue contents, including lymph nodes, along the

defined boundaries of one or two contiguous neck levels

[15]. This very limited neck dissection has been proposed to

be oncologically sound for two indications: elective treat-

ment of the clinically negative (N0) neck and treatment of

persistent neck disease (N?) after chemoradiotherapy.

In clinical practice, the N0 neck exists when there is no

evidence of metastasis on physical examination or on

imaging studies. The most recent techniques of computed

tomography (CT), magnetic resonance imaging (MRI),

ultrasonography, positron emission tomography (PET) and

ultrasound-guided fine-needle aspiration biopsy (UGFNAB)

have shown good diagnostic efficacy (sensitivity & 70 %

and specificity & 90 %) in detecting non palpable metas-

tases [17]. With great strides in staging modalities and

technology, the connotation of an N0 neck confirmed that

following appropriate imaging has changed through stage

migration. Many necks classified as N0 in the past would

now be upstaged to N? due to the improved detection rate.

An important factor in the consideration as to whether to

perform elective neck dissection is the rate of occult

metastasis for a particular primary tumor. The work of

Weiss et al. [18] has established a threshold of a 20 %

possibility of cervical metastasis as the indication for

elective treatment of the neck in HNSCC. Others have

suggested that this threshold be lowered to 15 %, consid-

ering that most elective operations currently performed are

SND, resulting in much less morbidity and better func-

tional outcome than the more radical procedures employed

in the past for this purpose [19].


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Similar to the basis for SND, the oncologic basis for

SSND derives from the fact that lymphatic flow follows an

orderly and predictable path in the neck, and also from

analysis of histopathological findings in comprehensive

neck dissection specimens. The underlying principle is that

the pattern of neck metastasis from HNSCCs is predictable

based on the location of the primary lesion [20, 21].

The landmark study reported by Shah [20] based on

1,119 classic RND on 1,081 previously untreated patients

included 343 patients with a clinical N0 neck. Focusing

only on this group, the results were as follows: the most

common metastatic site for all tumors was the ipsilateral

level II. Oral cavity tumors most often metastasized to

levels I–III, with levels IV or V rarely involved (9 and 2 %

of cases, respectively). Oropharyngeal tumors most com-

monly metastasized to levels II–IV, and levels I and V

were involved in only 7 % of cases. Hypopharyngeal

tumors metastasized mostly to levels II–IV, and none of the

specimens had metastasis in levels I and V. Laryngeal

tumors metastasized to levels II–IV, with levels I and V

involved in 14 and 7 % of cases, respectively. One of the

important findings of Shah’s study was that in the absence

of metastasis to levels I–IV, level V nodes were never

positive. Based upon these studies, the vast majority of

surgeons now perform SND for the N0 neck.

Further studies have evaluated neck dissection speci-

mens from clinically negative necks to determine which

levels and sublevels are likely to contain metastatic lymph

nodes. The controversy over the need to include the dis-

section of sublevel IIB has represented an interesting step

forward in minimizing shoulder morbidity associated with

dissection of the spinal accessory nerve, which traverses

this sublevel. Dissection of sublevel IIB involves traction

on the spinal accessory nerve as well as devascularization,

with associated potential morbidity. Santoro et al. [22]

reported that among 148 neck dissections performed, sub-

level IIB nodes were positive for metastases in 3.3 % of

cases. When reported by classification for N0 and N?

necks, the incidence of positive sublevel IIB nodes was 2

and 5 %, respectively. All cases with metastases at sub-

level IIB also showed metastases at sublevel IIA, with a

statistically significant association between the presence of

nodal metastases at sublevel IIB and those at sublevel IIA.

A review from seven prospective, multi-institutional,

pathologic, and molecular analyses of neck dissection

specimens, obtained from 272 patients with laryngeal

squamous cell carcinoma and clinically negative necks,

revealed only 4 (1.4 %) patients with positive lymph nodes

at sublevel IIB. All patients with positive nodes at sublevel

IIB had positive nodes at other levels [23].

Paleri et al. [24] conducted a prospective study of 50

patients and a systematic review of the literature to identify

the incidence of occult metastases in the lymph nodes of

sublevel IIB in HNSCC among patients whose neck was

staged N0 by physical and radiologic examination. The

review identified 14 articles with a total cohort of 903 necks

suitable for inclusion. The overall incidence of metastatic

disease at this sublevel in the context of an N0 neck from

any site was 2.0 % (18 of 903). The incidence of occult

metastatic disease in sublevel IIB for oral cavity, oropha-

ryngeal, and laryngeal cancer was 3.9 % (11 of 279), 5.2 %

(5 of 96), and 0.4 % (1 of 230) patients, respectively.

Contralateral positive nodes (0.9 %) and isolated metasta-

ses (0.3 %) at this sublevel were also rare. The authors

concluded that routine dissection of sublevel IIB is not

required for the surgical treatment of HNSCC with a clin-

ically negative neck. Consequently, it is conceivable that

spinal accessory nerve dysfunction can be minimized and

operative time diminished without adversely affecting

oncologic outcomes. However, to date, this has not been

verified by appropriate outcomes studies. Similar anatomic

and histopathological studies have been conducted with

regard to level IV in laryngeal cancer. In the review pre-

viously mentioned, Ferlito et al. [23] collected data from

three prospective, multi-institutional, pathologic, and

molecular studies of neck dissection specimens, which

included 175 patients with laryngeal squamous carcinoma

and clinically negative necks. Among these patients, only

six (3.4 %) patients had positive nodes at level IV. Redaelli

de Zinis et al. [25], in a study on 402 consecutive patients

with supraglottic squamous cell carcinoma, reported that

level IV was involved only in association with level II

and/or level III metastasis, whereas levels I and V were

rarely involved when overt metastases were present at other

levels and never in association with occult metastases. In a

retrospective study of 43 patients with laryngeal carcinoma

who underwent elective lateral neck dissection, only 1

patient had level IV metastases. That patient also had

metastases at level II. The authors concluded that dissection

of level IV might not always be necessary in patients with

cancer of the larynx and a clinically N0 neck [26]. Simi-

larly, in a review of 58 patients who underwent elective

posterolateral (levels II–V) and lateral neck dissection

(levels II–IV) for supraglottic carcinoma no isolated level

IV lymph node metastases were encountered [27]. The

findings of these studies suggest that dissection of level IV

lymph nodes may not be justified for elective neck dissec-

tion of stage N0 laryngeal squamous cell carcinoma.

Potential complications such as chylous fistula or phrenic

nerve injury may be avoided and operative time reduced

without adversely affecting oncologic results [23]. Taking

into account that in the supraglottic larynx lymphatic

pathways are bilateral for midline lesions, generally neck

dissections need to be bilateral for supraglottic lesions.

Thus, a further advantage, in time and potential morbidity,

is gained by the more limited dissections.


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Another potential level to be preserved during neck

dissection is level III in oral squamous cell carcinomas. In

a review of histopathological findings of 439 patients with

oral and oropharyngeal carcinoma who underwent a com-

prehensive or SND, Woolgar [28] described the typical

pattern of nodal metastasis in these tumors as an ‘‘inverted

cone’’, with maximal disease volume and maximal extra-

capsular spread at levels I and II and with progressive

diminution inferiorly. ‘‘Skip’’ metastasis to level III

(metastases in level III with no metastases in levels I or II)

were found in 10 % of patients. In a study of 226 neck

dissections performed for oral cavity squamous cell carci-

noma, with clinically N0 or N1 necks, skip metastases to

level III or level IV occurred in 14 cases (6 %), which

would not have been removed in case of a SSND levels I–II

[29]. In another study that included fifty-two consecutive

patients with clinical T1–T4 N0 stage oral tongue carci-

noma who underwent excision of the primary tumor with

neck dissection (levels I–IV), the incidence of isolated

pathologic level III or IV involvement and isolated nodal

recurrence at levels III and IV was analyzed. Isolated

microscopic level III involvement occurred in two (3.8 %)

patients, and isolated level IV involvement was found in

one (1.9 %) patient. One of these patients had recurrence in

level II but none had recurrence in level III or IV [30].

Given the low incidence of isolated nodal metastasis at

level III in clinically N0 oral squamous cell carcinoma, the

routine inclusion of this level in SND may not be justified.

Based on recent works, it appears that further refinement

can be made to level I dissection. It has been recognized for a

long time that the submandibular salivary gland has no in-

traparenchymal lymph nodes, and intraglandular spread in

HNSCC occurs through extension from a locally involved

lymph node or the primary tumor. The incidence of metastatic

disease based on pathological examination ranges between 1

and 5 % in N? disease and 0 % in N0 disease [31–33].

Leaving the gland behind does not seem to impair access and

permits comprehensive clearance of sublevels IA and IB [34].

One prospective study has shown that this does not lead to

poor outcomes [35]. In the chemoradiation era where xero-

stomia is a significant cause of impaired quality of life [36],

this additional refinement needs to be explored further.

Patients with some tumors of the floor of the mouth, however,

may benefit from removal of the submandibular gland simply

to avoid obstruction of the duct and resultant sialadenitis,

unless Wharton’s duct can be identified and transposed

without compromising resection of the primary tumor.

In general, we can conclude that SSND could have a

role in tumors of the oral cavity with clinically negative

cervical nodes (SSND I–II), and also in laryngeal tumors

with clinically negative neck (SSND II–III). In both cases,

sublevel IIB may not require routine dissection if no nodal

metastasis are found in other levels.

The N? neck after chemoradiotherapy

Another situation in which SSND could be indicated is the

treatment of the N? neck after chemoradiotherapy. In this

setting, although neck dissection is not routinely recom-

mended for complete responders, SND is oncologically

feasible with minimal morbidity in the presence of residual

disease [37]. The feasibility of SSND in these cases was first

demonstrated by Robbins et al. [15]. Additional evidence

comes from a recent report, in which 104 HNSCC patients

undergoing neck dissection after chemoradiotherapy were

studied, comparing CT findings after chemoradiotherapy

with histopathological examination of the neck dissection

specimen [38]. Primary location and CT findings were used

to design theoretical SND or SSND in patients who then

underwent comprehensive neck dissection to determine

whether the proposed selective procedures would have

removed all metastatic disease. Neck dissections were

positive in 20 (19 %) of 104 patients, corresponding to 20

hemi-neck dissections, 31 neck levels, and 53 lymph nodes.

The negative predictive value for CT was 95 percent. SND

or SSND, guided by level specific CT findings and limited to

necks with post treatment partial response at one level,

would have captured all disease in 52 (95 %) of 55 and 51

(93 %) of 55 hemi-necks, respectively. This work shows that

CT reliably identifies low risk neck levels that do not require

dissection, thus permitting SSND in partial response patients

with limited residual disease. As post-treatment CT-PET

scans achieve negative predictive values of 98 % for resid-

ual disease [39], the case for limiting surgical morbidity by

performing SSND is very strong.

Finally, although SND entails less morbidity than

comprehensive neck dissection, complications and seque-

lae exist which potentially can be reduced with more

conservative procedures. Thus, functional and aesthetic

results were evaluated in 52 patients receiving SND by

Teymoortash et al. [40]. Some SND-related complications

were observed including injury to the thoracic duct (4 %),

persistent lymphedema (19 %), and sensitivity distur-

bances related to the skin incision (65.4 %) at a minimum

of 6 months follow-up. With regard to head, neck, and

shoulder function, no significant differences were noticed

by 82 % of patients for arm abduction, 84 % for head

rotation, and 79 % for lateral head inclination.

Results of superselective neck dissection

Several authors have reported similar rates of regional

control and survival after selective and comprehensive

neck dissection in patients treated primarily with surgery

[41–43]. However, few studies have addressed the onco-

logic safety of SSND in HNSCC.


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In a prospective search to find a less invasive method of

neck treatment, Leon et al. [44] evaluated the results of

intraoperative pathologic control (frozen section analysis)

of levels II–III in a group of patients with laryngeal car-

cinoma. When intraoperative frozen sections were positive,

dissection of levels IV and V was completed. Although the

sensitivity of frozen sections for the detection of occult

metastases was only 76 %, and in 7 additional cases tumor

was found in the postoperative study, there was no regional

relapse in any of the SSND, leading to the conclusion that

this procedure is an effective method for elective treatment

of the N0 neck in patients with laryngeal carcinoma.

Ambrosch et al. [45] performed neck dissections limited

to levels II and III in the majority of patients with laryngeal

cancer and clinically negative neck disease undergoing

transoral laser resection although it was only after publi-

cation that this targeted procedure became referred to as a

SSND. There were 503 previously untreated patients

undergoing 711 SNDs as a part of initial therapy for

squamous cell carcinoma of the larynx, oral cavity, oro-

pharynx, and hypopharynx. Lymph nodes were pathologi-

cally negative in 249 and positive in 254 patients.

Postoperative radiotherapy was administered to 14.5 % of

the node-negative and 62.2 % of the node-positive patients.

The median follow-up interval was 41 months. Three year

regional recurrence rates estimated according to Kaplan–

Meier were as follows: pN0 4.7 %, pN1 4.9 %, and pN2

12.1 %. A comparison of recurrence rates with respect to

the extent of neck disease and postoperative radiotherapy

demonstrated a tendency towards improved regional con-

trol in irradiated patients with one metastasis and distinctly

improved regional control in patients with multiple

metastases or metastases with extracapsular spread. The

authors concluded that the results achieved with SND

(actually SSND) compare favorably with the results

reported for MRND, and suggested that the application of

SND might be extended to more advanced neck disease.

More recently, Jia et al. [46] performed 122 SSND

(levels II and III) on 68 patients with clinically N0 supra-

glottic carcinoma. The rate of occult metastasis was 30.9 %

(21 of 68), and metastases in sublevel IIB were not found in

any patient, on either side of the neck. Five patients

developed neck recurrence, none of which was in sublevel

IIB. The authors concluded that when SND is done in

patients with SCC of the supraglottic larynx with N0 neck,

SSND removing lymph nodes in sublevel IIA and level III

may be adequate. However, when SSND is used as part of

the primary treatment, it is important to point out that the

presence of positive nodal disease found within the neck

dissection specimen is often an indication for post-opera-

tive adjuvant radiation therapy.

Finally, the results of submandibular neck dissection

(level I) versus MRND have been reported by Yanai et al.

[47] in patients with oral squamous cell carcinoma with or

without nodal metastasis. They identified 229 patients with

clinically N0 necks and 68 with clinically N1 necks in level

I. Most of the patients who had advanced disease (stage III

or IV) received neoadjuvant chemoradiotherapy, but the

number of patients who received it was well balanced

between both arms. In clinically node-negative necks, the

regional control rates were 85.2 % with submandibular

neck dissection alone and 83.3 % with MRND. Compari-

son of the 5-year disease specific survival rates (86.5 vs.

87.0 %, respectively) indicated no statistical difference

between the groups. In clinically N1 necks, the regional

control rates were 81.3 % with submandibular neck dis-

section and 83.0 % with RND, and the disease specific

survival rates were 81.3 and 80.0 %, respectively. Com-

parison of the type of neck dissection was not significantly

different for regional disease control and disease specific

survival. Most of the regional recurrences in patients who

underwent submandibular neck dissection, as well as in

patients with N0 necks, were detected at sublevel IIA in the

ipsilateral neck early in follow-up. This suggests that the

inclusion of sublevel IIA in the dissection could avoid most

of neck recurrences, and that, in experienced hands, SSND

of levels I–II could be appropriate in patients with oral

cavity cancers with an N0 neck.

The concept of SSND can be extended to patients with

residual neck disease after chemoradiation [14, 16, 48]. In

a series of 177 patients with N? disease, 73 had clinical

evidence of residual adenopathy involving only one neck

level after treatment with chemoradiotherapy. Within this

subset, 54 patients subsequently underwent a salvage neck

dissection and 2 had evidence of pathologic disease

extending beyond the single neck level. One had disease in

a contiguous neck level, and the other had disease in a

noncontiguous level. As a consequence, the use of SSND

with removal of only two contiguous neck levels based on

preoperative image studies (CT, MRI, or PET) would have

encompassed known disease in all but one patient [48].

Robbins et al. [15] compared the results of different types

of neck dissection in a series of 240 patients treated with

chemoradiotherapy. Among the total group of patients, 106

neck dissections were performed on 84 patients who had

initially bulky nodal disease. Regional failure occurred in

17 % of the patients who had modified RND, 5 % of the

patients who had SND, and none of the patients who had

SSND, but the different subsets were not equivalent in

number. In addition, the rates of overall survival and distant

metastases were not significantly different among the three

neck dissection subsets [15].

Robbins et al. [16], in another study, reported additional

data to support the efficacy of SSND following chemora-

diation. A retrospective analysis of the databases from two

institutions indicated that 35 SSNDs were performed on 30


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patients following chemoradiation as either a planned or

early salvage intervention. The results indicated that over a

median follow-up of 33 (range 8–72) months, eight patients

developed recurrent disease (three primary, five distant) but

there were no isolated recurrences in the neck. The pro-

jected 5-year disease specific survival rate for the group

was 60 %.

The use of frozen section in the post chemoradiation

setting is probably not as reliable as in other circumstances,

because many initially invaded lymph nodes have been

‘‘sterilized,’’ and the definitive pathologic answer frequently

requires immunohistochemistry.

Conclusions

The data from the reviewed studies suggest that SSND with

the use of intraoperative frozen sections may achieve

regional disease control that is comparable to more

extensive neck dissections in selected patients with lar-

yngeal cancer (removal of IIA–III) and oral cavity cancer

(removal of I–IIA) among patients who present with a

clinically negative necks.

Not as much data is available for the efficacy of SSND

following chemoradiotherapy. However, the reports to date

suggest that SSND is a feasible therapeutic alternative for

patients with residual disease confined to a single neck level.

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Superselective neck dissection: rationale, indications, and results

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