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The evolution of surgery in the management

of neck metastases
Levoluzione della chirurgia nelle metastasi linfonodali laterocervicali
Department of Head and Neck Surgery, N.N. Blokhin Russian Cancer Research Center, Moscow, Russian Federation;
Department of Head and Neck Surgery, European Institute of Oncology, Milan, Italy; 3 Department of Oncology, I.M.
Sechenov Moscow Medical Academy, Moscow, Russian Federation

Key words Parole chiave

Neck Lymph nodes Neck dissection Classification Collo Linfonodi Linfoadenoctomia laterocervicale
History Evolution Classificazione Storia

Summary Riassunto
In spite of advancement in science, molecular medicine and Nonostante lavvento della medicina molecolare, la
target therapies, surgical treatment of metastases using diffe- chirurgia (con le varie tecniche dagli svuotamenti radicali
rent techniques, from selective neck dissection to extended ra- a quelli selettivi) rappresenta ancora oggi il pi impor-
dical neck dissections, form a major part in the management of tante presidio terapeutico delle metastasi linfonodali nei
neck metastases. This is due to the fact that, so far, there is no carcinomi squamocellulari della testa e collo. Esse infatti
treatment more effective for resectable neck metastases, than rappresentano il fattore prognostico pi importante in
surgery. Since most head and neck cancer patients die due to queste neoplasie. Questa review si propone di illustrare il
loco-regional progression of disease, and a very large majority percorso fatto dai chirurghi e dagli oncologi cervico-
of them do not live long enough to develop distant metastases, facciali nei centanni trascorsi dalla pubblicazione di Crile,
the status of neck lymph nodes remains the single most impor- che per primo descrisse tecnica e risultati dello svuota-
tant prognostic factor, in these cases. In the 100 years since mento laterocervicale. Inizialmente, venivano praticate
George Washington Crile described Radical Neck Dissection, tecniche chirurgiche demolitive; successivamente sono
we now have a much better understanding of the biological state utilizzate metodiche pi rispettose della funzione.
and clinical behaviour of neck metastases. This has ultimately Negli ultimi anni lo studio del linfonodo sentinella e la
led to the conservative approaches of selective neck dissec- mappatura del flusso linfatico hanno permesso di meglio
tions depending on the primary site of the tumour, type of tu- conoscerne le vie di diffusione e di personalizzare la terapia
mour and the characteristic features of the metastases themsel- delle aree linfatiche, riducendo la morbilit legata a questi
ves. A search of the literature on neck lymph nodes and neck interventi. Nel futuro, la diagnostica molecolare e le terapie
dissections, on the internet and in old publications, not availa- mirate ci consentiranno di migliorare ulteriormente i risul-
ble in the electronic media, has been carried out. Using this as tati oncologici e funzionali.
the basis, we arranged, in sequence, the dates of various land-
marks in the treatment of head and neck cancer related to neck
dissections to emphasize the overall process of evolution of
neck dissection thereby showing how the field of head and
neck surgery has travelled a long way from radical neck dis-
section to its modifications and further to selective neck dis-
sections and sentinel node biopsies. The present understanding
of the patterns of neck metastases enables us not only to ade-
quately treat the neck metastases, but also to diagnose meta-
stases from unknown primaries. Therefore, depending on the
site of the primary tumour, it is now easy to predict the most
probable route of metastatic spread and vice versa. This has
enabled us to adopt modified and selective neck dissections
which have ultimately led to a dramatic reduction in morbidity
and almost eliminated mortality due to neck dissection. In the
near future, molecular diagnostics and targeted therapies for
treating metastases should be able to further reduce the burden
of head and neck cancer.


In ancient times, Hippocrates and Aristotle men-

tioned the presence of lymph vessels. In the follow-
ing centuries, no mention was made of lymphatic
vessels or nodes, until the 17th Century.

Lymphatic network: Anatomical studies

1622: the Italian anatomist. in Pavia. Gaspar Asellius

(Fig. 1) rediscovered the lymphatic system 1 2. He
demonstrated the functional relationship between
food consumption and filling of mesenteric lymphat-
ic vessels in dogs (Fig. 2).
1692: Antony Nuck studied the lymphatic network
introducing mercury into the lymphatic vessels of ca-
davers 1 2.
1787: Paolo Mascagni published Vasorum lymphati-
corum corporis humani historia et iconographia.
This important publication focused on the first sys-
tematic description of the human lymphatic system 1 2.
1909: Poirer 3 published a treatise on the human
anatomy with a description of the lymphatic network.
1930: H.A. Trotter described the surgical anatomy of

Fig. 2. Mesenteric lymph vessels (copy of Gaspar Asellius


head and neck lymphatics, indispensable help for

surgeons that perform neck dissections 4.
1938: H. Rouviere elaborated the classification of
neck lymph nodes, based on the topographic anato-
my of the neck, in a volume Anatomy of human lym-
phatic system 5, on which, still now, we base our
clinical practice 6.

Lymphatic network: functional studies

In those same years, several Authors, as reported by

Werner and by Wise 1 2, studied the lymphatic system
from a functional point of view.
1840: A. Cooper found the presence of breast cancer
cells in the lymphatic vessels, thereby demonstrating
the lymphogenic spread of malignant tumours.
1860: R. Virchow, continuing Coopers studies,
showed that lymph nodes form a barrier preventing
dissemination of tumoural cells.
1865: H.F. Le Dran reproduced the work of Cooper
Fig. 1. Gaspar Asellius (Source: Human Lymphatic sys- and confirmed his conclusions.
tem, B.N. Uskov, Medgis, Moscow, 1948).
Later, these studies were abandoned and only in the


last fifteen years have they been restarted thanks to reported that oncological results of such an approach
the introduction, in clinical practice, of Sentinel were good.
Node Biopsy (SNB). 1906: G.W, Crile (Fig. 3) described the technique of
2000-2001: T. Soahib 7 and F. Chiesa 8 reported their radical neck dissection 10. In his paper, he reported on
experience in SNB, on head and neck squamous cell 132 radical neck dissections in which the boundaries
carcinoma (SCC), and proved its reliability. of resection were the clavicle, the strap muscles and
2006: C. De Cicco published a paper on the use of the posterior border of the sternocleidomastoid mus-
dynamic lymphoscintigraphy (Lymphatic Mapping) cle. He also removed the sternocleidomastoid mus-
to identify the nodes reached by the lymphatic stream cle, posterior belly of the digastric muscle, internal
from the tumour in order to tailor a selective dissec- jugular vein and accessory nerve but left the platys-
tion on each patient with clinically negative necks ma intact. G.W. Criles experience was a milestone in
(cN0) 9. the development of neck dissection in the 20th Centu-
About a third of the human lymph nodes are local- ry, because unlike Jawdynskis report, his paper and
ized in the neck. Head and neck carcinomas mostly his ideas spread rapidly all over the world.
exhibit lymphogenic metastatic spread. Metastases in 1911: R.H. Vanakh, described the so-called collar in-
the neck are mostly due to a primary tumour arising cision for removal of carcinoma of the lower lip 20.
in the head or neck region. The enormous amount of Through this incision, he removed both the sub-
experience gained by surgeons worldwide has led to mandibular salivary glands, and submandibular and
the understanding that patterns of metastatic spread submental lymph nodes. This technique was later on
of these cancers depend on the topography of the referred to as Vanakh surgery.
lymphatic system 9-11. 1913: H. Morestin described an operation with a cu-
taneous access that he called incision stellaire 21.
Unlike Crile, he preserved the sternocleidomastoid
Neck dissection muscle, internal jugular vein and accessory nerve. He
removed the upper jugular lymph nodes along the ac-
Improvements in the knowledge of the nature of cessory nerve, now classified as level IIB 22-26. Nei-
metastatic disease led surgeons to remove neck
metastases and the first reports were published in the
later part of the 19th Century. Since then, surgery still
remains the main modality of treatment of neck
metastases. The major steps are outlined below.
1847: J.C. Warren reported an experimental dissec-
tion of carcinoma in the neck 12.
1880: T. Kocher described the surgical removal of a
tumour of the tongue en bloc with the regional lymph
nodes using a mandibulotomy approach 13.
1885: H. Butlin described the resection of carcinoma
of tongue with dissection of cervical lymph nodes 14.
1888: The Polish surgeon F. Jawdynski 15 performed a
radical neck dissection using a surgical technique sim-
ilar to that described by G.W. Crile 18 years later 16.
His paper was published in Polish, in a Polish jour-
nal, therefore only a few surgeons became acquaint-
ed with this technique.
1894: The Russian surgeon M. Regulskiy underlined
the importance of removing neck lymph nodes, what-
ever their condition (metastatic or not), in cancer of
the lower lip 17 18.
1901: J. Solis-Cohen emphasized the need for neck
dissection irrespective of the presence or absence of
clinically palpable metastases from laryngeal carci-
noma 19.
1905: H. Butlin 14 removed a cancer of the tongue to-
gether with submandibular salivary gland and lymph
nodes, part of the omohyoid muscle, upper jugular
group of lymph nodes, platysma and part of the in- Fig. 3. George Washington Crile.
ternal jugular vein if it was infiltrated by the tumour.


ther Crile nor Morestin removed the posterior supra-

clavicular nodes (now level V).
1927: J. Roux-Berger described a technical variant of
Criles operation: he removed the stylohyoid muscle
and the posterior belly of the digastric muscle to ob-
tain better access to the upper jugular chain and ac-
cessory nodes 27. R. Bernard emphasized the onco-
logical role of Criles operation and underlined the
importance of Morestins dissection enlarged to the
accessory nodes 28.
In this period, Soviet surgeons developed good ex-
pertise in neck dissection and published several pa-
pers, the more important are outlined herewith:
1928: P.A. Hertzen performed neck dissections pre-
serving the internal jugular vein and sternocleido-
mastoid muscle in cases without metastatic infiltra-
tion of these structures. He emphasized that, for
tongue cancer, taking into consideration the charac-
teristic features of lymphatic flow and topographic
anatomy of neck lymph nodes, all nodes along the in-
ternal jugular vein should be removed apart from re-
moving all the tissue from the base of tongue 29.
1929: N.N. Petrov published his experience on radical
neck dissection in 32 patients with head and neck can-
cer and emphasized that surgery is more effective than
radiotherapy in the management of neck metastases 30.
1940: I.E. Davydov treated laryngeal cancers pre-
serving the internal jugular vein, sternocleidomastoid
muscle and accessory nerve if there was no metas-
tases involving these structures 31. He removed only
the lymph nodes above the intersection of the stern- Fig. 4. Neck lymph node levels according to the AAO-
ocleidomastoid muscle and omohyoid muscle, and HNS.
left those at levels IV and V.
After the second world war, neck dissection was re-
visited both in Europe and in the USA:
1945: M. Dargent described bilateral neck dissection
preserving the internal jugular veins as curative treat-
ment 32.
1951: H. Martin emphasized the importance of neck
dissections. He published the experience of 1450 rad-
ical neck dissections performed at the Memorial Hos-
pital from 1928 to 1950 33. He was responsible for the
wide dissemination of the radical neck dissection
technique all over the world.
1960: E.A. Gould underlined the usefulness of intra-
operative histological examination of nodes 34. He re-
ported that in 1951, while performing a parotidecto-
my, he sent, for frozen section, a node which looked
normal, located at the junction of the anterior and
posterior branches of the facial vein. The histological
report was lymph node with metastatic tumour. He
called this node Sentinel Node. From then on intra-
operative examination of the facial vein guided their
decision whether to perform radical neck dissection
during parotidectomy. Fig. 5. Lymph nodes in and around the neck (Source: Hu-
man Lymphatic system, B.N. Uskov, Medgis, Moscow,
1962: O. Suarez, described functional neck dissec-
tion, now called modified radical neck dissection 35 36.

Table I. Anatomical structures defining the boundaries of neck lymph node levels as per the AAOHNS.

Levels Lymph node Boundaries Comments Primary tumour site


Superior symphysis of mandible Only submental lymph nodes Lower lip, anterior part of oral
IA Submental Lateral anterior bellies of digastric muscles belong to this level cavity, floor of mouth, anterior
Inferior body of hyoid bone portion of alveolar part of mandible

Superior body of mandible When metastases are present in Oral cavity, anterior portion of nasal
IB Submandibular Anterior anterior belly of digastric muscle this level, the submandibular gland cavity, soft tissues of the face,
Posterior stylohyoid muscle is also usually removed during submandibular gland
Inferior posterior belly of digastric muscle neck dissection

Superior skull base

IIA Anterior stylohyoid muscle The lymph nodes around the Oropharynx (including retromolar
Posterior accessory nerve internal jugular vein in this region region, soft palate, tonsils), thyroid
Upper jugular Inferior horizontal plane defined by located anterior to the accessory gland, parotid gland
(subdivided into the inferior body of hyoid bone nerve belong to this level
two sublevels)
Superior skull base
IIB Anterior accessory nerve The lymph nodes around the Oral cavity, nasal cavity, oropharynx
Posterior lateral border of the internal jugular vein in this region (including retromolar region, soft
sternocleidomastoid muscle located posterior to the accessory palate, tonsils), nasopharynx,
Inferior horizontal plane defined by nerve belong to this level hypopharynx, parotid gland
the inferior body of hyoid bone

Superior horizontal plane defined by the inferior body of hyoid bone These lymph nodes are located Oral cavity, oropharynx,
III Middle jugular Anterior medial border of the sternocleidomastoid muscle around the internal jugular vein nasopharynx, hypopharynx, larynx,
Posterior lateral border of the sternocleidomastoid muscle, branches of cervical plexus in this region thyroid gland
Inferior horizontal plane defined by the inferior border of cricoid cartilage

Superior horizontal plane defined by the inferior border of cricoid cartilage These lymph nodes are located
Anterior medial border of the sternocleidomastoid muscle around the internal jugular vein in Hypopharynx, thyroid gland, larynx,
IV Lower jugular Posterior lateral border of the sternocleidomastoid muscle, branches of cervical plexus this region. The Virchow node cervical oesophagus, stomach
Inferior clavicle which is significant for gastric
cancer also belongs to this level

Posterior triangle Superior apex of convergence of the sternocleidomastoid and trapezius muscles Lymph nodes along the lower Nasopharynx, oropharynx, skin of
VA (subdivided into Anterior lateral border of the sternocleidomastoid muscle, branches of cervical plexus portion of accessory nerve posterior neck, skin of the scalp
two sublevels; the Posterior trapezius muscle
demarcation line is Inferior horizontal plane defined by the inferior border of cricoid cartilage
the horizontal
plane defined by the Superior horizontal plane defined by the inferior border of cricoid cartilage Lymph nodes along the
VB inferior border of Anterior lateral border of the sternocleidomastoid muscle, branches of cervical plexus transverse artery and other Thyroid gland
cricoid cartilage) Posterior anterior border of trapezius muscle supraclavicular nodes,
Inferior clavicle except Virchows node

VI Anterior Superior hyoid bone This group includes pre-

compartment Lateral common carotid arteries paratracheal, prelaryngeal, Thyroid gland, glottic, subglottic
Inferior suprasternal notch precricoid, perithyroidal lymph larynx, apex of piriform sinus,
nodes and the nodes along the cervical oesophagus
recurrent laryngeal nerves

Table II. Classification of neck dissections (AAO-HNS) 25.

Surgery Structures removed

Radical Neck Dissection Lymph node levels I-V, sternocleidomastoid muscle, internal jugular vein and ac-
cessory nerve
Extended Neck Dissection Lymph node levels I-V, sternocleidomastoid muscle, internal jugular vein and ac-
cessory nerve + (plus) at least one lymphatic or non-lymphatic
structure not sacrificed during radical neck dissection (parapharyngeal nodes, su-
perior mediastinal nodes, perifacial nodes, carotid artery,
hypoglossal nerve, vagus nerve, paraspinal muscles, etc.)
Modified Radical Neck Dissection Radical neck dissection - (minus) at least one of the three major structures name-
ly sternocleidomastoid muscle, internal jugular vein or accessory
nerve. The structure preserved should be specifically named.
Selective Neck Dissection At least one of the six lymph node levels/sublevels preserved. None of the struc-
tures namely sternocleidomastoid muscle, internal jugular vein
and accessory nerve are sacrificed (the removed levels or sublevels should be
mentioned within parentheses: I-III, II-VI, VI etc.)

1967: E. Bocca described in detail the surgical steps included radical neck dissection, modified radical
of the functional neck dissection 37; he led to this op- neck dissection, extended neck dissection and se-
eration becoming popularall over the world 38 39, and lective neck dissections which were subdivided in-
which is, today, usually defined as Suarez-Bocca to supraomohyoid, anterolateral, lateral and pos-
technique. terolateral neck dissections. The neck levels and
1969: Two Soviet surgeons (A.I. Paches and G.V. their corresponding lymph node groups are shown
Falileev) described the Fascial compartment dissec- in Figures 4 and 5, respectively, and the most com-
tion of neck tissue which corresponds to functional mon related primary sites of tumours are shown in
neck dissection 40. Up to now, in the Russian speak- Table I.
ing countries, the term Fascial compartment dissec- 2002: The latest classification of neck dissections 25
tion of neck tissue is widely in use to define conser- proposed by the AAO-HNS committee (Table II) is
vative functional surgery, even if all modified types quite simple to understand and is based on the neck
of operations, from selective to extended neck dis- lymph node levels. It includes the following changes
sections, are routinely performed, while Criles op- to the previous classification:
eration indicates a radical neck dissection. 1. Any lymph node group outside the neck would be
1972: R. Lindberg published a study on the distribu- referred to by the name of that specific group,
tion of neck metastases; it was another landmark and even though many Authors suggest defining the
formed the basis for further evolution of neck dissec- tracheo-oesophageal and superior mediastinal
tions 41. nodes as level VII.
1981: J. Shah recommended modified neck dissec- 2. Sublevels a and b were introduced in levels I, II
tion for N0 neck and radical neck dissection for clin- and IV.
ically positive necks 42. 3. The structure(s) preserved in modified radical
1988: The American Academy of Otorhinolaryngolo- neck dissection should be specifically mentioned
gy Head and Neck Surgery (AAO-HNS) initiated in surgical reports.
the neck dissection classification project. An ad hoc 4. The levels removed in selective neck dissections
committee of the newly formed American Head and should be quoted within brackets. Each dissection
Neck Society (AHNS) was convened to review, at (Table II) should be defined by the levels re-
regular intervals, the classification scheme 22. moved instead of the traditional classification
1990: J. Shah classified the deep lymph nodes of the (supraomohyoid, lateral, posterolateral and ante-
neck into five different levels assigned Roman nu- rior neck dissection).
merals from I to V 43. This was another landmark, as
the present classification of neck lymph nodes is ful-
ly based on that launched in this paper. Conclusion
1991: AAO-HNS made the first attempt to stan-
dardize neck dissection terminology 23. This classi- Knowledge of the patterns of metastatic spread of
fication added level VI to the topography of cervi- head and neck cancers, development of modern
cal lymph nodes earlier proposed by J. Shah, and surgery, and advancement in imaging, cytology and


molecular medicine permit us to individualize the patterns of neck metastases enables us to tailor treat-
treatment of patients. Since Criles publication, in ment of neck metastases on each patient. This has ul-
1906, head and neck surgeons and oncologists from timately led to a dramatic reduction in morbidity,
all over the world have accumulated enormous expe- with almost no mortality related to neck dissection.
rience in the management of neck metastases. In this We believe that, in the near future, molecular diag-
period, a long journey has been undertaken from rad- nostics and targeted therapies will be able to reduce
ical neck dissection to selective neck dissections, and the burden of head and neck cancer.
sentinel node biopsies. Our present knowledge of

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n Received: November 4, 2006

Accepted: November 20, 2006

n Address for correspondence: Dr. S. Subramanian, Surgical

Oncologist and Clinical Trials Coordinator, Department of
Head and Neck Surgery, N.N. Blokhin Russian Cancer Re-
search Center, 24, Kashirskoye Shosse, Moscow, Russian
Federation 115478. Fax: +7 495 3241930. E-mail: drso-