Kristen Pytynia Abstract
The presence of regional metastatic lymphadenopathy from mucosal squamous cell carcinoma decreases survival by 50%. The management and control of regional metastasis is paramount to both oncological and functional long-term outcomes. The supraomohyoid neck dissection gained popularity in the 1970s and 1980s as an alternative to the functionally debilitating radical neck dissection. Supraomohyoid neck dissection consists of removing lymph nodes in levels Ia, Ib, II, and III, while preserving the sternocleidomastoid muscle, the internal jugular vein, and the spinal accessory nerve. The omohyoid muscle is the lower limit of dissection. Level IIb can be included in the resection based on whether there is disease present in level IIa. A supraomohyoid neck dissection is indicated for patients with a clinically N0 neck, or with low-volume neck disease from a primary tumor that typically drains into levels I, II, or III. Most commonly, this procedure is performed for the management of oral cavity cancers.
Keywords: supraomohyoid neck dissection, occult disease, radical neck dissection, oral cavity, functional outcome
9.1 History and Rationale
The evolution of the surgical management of the neck is a fascinating tale, one which we briefly summarize here and note that avid historians have written more extensively on the topic.1 In 1906, Crile proposed radical resection of all of the lymph nodes of the neck, including the sternocleidomastoid muscle, internal jugular vein, and spinal accessory nerve, and the lymph nodes from the mastoid to the clavicle to ensure an oncological sound procedure.2 The sternocleidomastoid muscle, the internal jugular vein, and the accessory nerve were considered the anatomical borders of the fat packet containing the lymph nodes of the neck. Resection of the muscle, vein, and nerve improved access to the lymph nodes and ensured oncological removal. This procedure, which became known as radical neck dissection, was in line with the then contemporary surgical practice—championed by Halstead, who theorized that cancer recurrences were the product of too conservative surgical resections. To give Crile credit, he apparently did question the need for the resection of uninvolved structures, but continued to recommend a more radical approach. Radical neck dissection has mortality and morbidity associated with it: carotid blowout syndrome, skin flap necrosis, severe facial edema due to bilateral internal jugular vein sacrifice, shoulder dysfunction, neck fibrosis, and chronic pain syndrome are some of the known risks and sequelae associated with the procedure.
During the first half of the 20th century, chemotherapy agents were discovered, and radiation was found to be effective against cancer cells. With these additions to the treatment armamentarium, as well as the recurrence of some cancers despite aggressive resection, surgeons questioned the efficacy and necessity of an overtly aggressive surgery. In 1951, Ward and Robben suggested that shoulder dysfunction could be avoided while maintaining oncological principles by preserving the spinal accessory nerve.3 They did recommend en bloc (contiguous) resection of the primary and cervical lymph nodes, as well as the sternocleidomastoid muscle and internal jugular vein, in order to remove the lymphatic vessels draining into the nodes. While preservation of the spinal accessory nerve improved some aspects of shoulder function, patients with large en bloc resections still had significant functional morbidity such as chronic pain, facial edema, and fibrosis. Furthermore, shoulder dysfunction was still a problem due to stretching of the accessory nerve. These debilitating morbidities associated with the procedure drove surgeons to consider other techniques.
Suarez and Bocca were two early champions of functional neck dissection, each publishing their experiences in the 1960s. There is some dispute over who originated the idea, as they had observed each other’s techniques. Suarez published his experience in the South American literature, and Bocca in the European literature. Bocca's technique relied on the anatomical knowledge of the fascial planes of the neck, which allowed removing the fat packet containing the cervical lymphatics while preserving the internal jugular vein, sternocleidomastoid muscle, and accessory nerve.4 He argued that it would be difficult for occult disease to cross these fascial barriers, and resection beyond those fascial barriers would not improve oncological outcome. Further, he advocated for this technique to be used on clinically positive lymph nodes, as long as they were not fixed to adjacent structures. Suarez's original article was published in Spanish, and was not widely recognized in the non-Spanish-speaking literature.5 The original Suarez article is difficult to find translated into English; therefore, Ferlito et al offer a passionate defense of Suarez's role in the development or functional neck dissection.6 He highlights Suarez's view that preservation of the sternocleidomastoid muscle protects the carotid artery from fatal rupture and the skin from necrosis. Their publications began a slow trend toward less radical surgery, in conjunction with the use of postoperative radiation. The modified radical neck dissection (MRND) was therefore any level I to IV or I to V neck dissection that preserved at least one structure: sternocleidomastoid muscle, internal jugular vein, or spinal accessory nerve.
In 1972, Lindberg characterized the location of positive nodes from upper aerodigestive tract of different sites of 2,044 previously untreated patients, essentially mapping the drainage patterns of various mucosal locations.7 This study showed that there are reliable and predictable patterns of lymphatic drainage and involvement of first echelon nodes. In particular, oral cavity cancer was noted to most frequently drain to nodes in levels I, II, and III, and the likelihood of lymph node involvement was noted to increase with primary tumor size (thickness for oral tongue). Understanding of the predicted pattern of nodal metastasis allowed for a more targeted surgical approach, and ushered in the era of selective neck dissections. The supraomo- hyoid neck dissection is a type of selective neck dissection that consists of removal of nodes in levels I, II, and III. The lower limit is the omohyoid muscle, and the sternocleidomastoid muscle, internal jugular vein, and accessory nerve are preserved.
In 1988, after years of attempting to standardize the approach for selective neck dissection, Byers et al published one of the larger series of selective neck dissections, 428 patients with primary cancers at different sites.8 This retrospective study examined the efficacy of supraomohyoid, MRND, and other selective neck dissections in patients with clinically negative (cN0) necks. Byers’ classic article examined the drainage patterns of different sites in the upper aerodigestive tract, and mapped where occult metastases were found in clinically node-negative necks. Focusing on oral cavity primary sites, he showed that disease from the oral cavity primarily spreads to levels I, II, or III, in concordance with Lindberg but focusing on microscopic (occult), and not clinically positive disease. Patients with different types of selective neck dissection fared well, with 15% neck failure rate, many on the contralateral undissected side. Therefore, Byers recommended that with careful patient selection, selective neck dissection can be both diagnostic (by identifying occult nodal disease) and therapeutic. Patients with multiple histopathologically positive nodes benefited from postoperative radiation.
In a subsequent study, Medina and Byers noted similar recurrence rates for patient with oral cavity cancer undergoing supraomohyoid neck dissection versus those receiving radical neck dissection.9 Spiro et al emphasized the importance of using the supraomohyoid neck dissection for low-volume disease, as well as postoperative radiation to decrease regional recurrence rates.10 Surgeons across the world continued to turn away from radical resections, resecting only those structures with direct tumor invasion. These classic studies were often retrospective, and many authors have attempted to study the question of effectiveness of supraomohyoid neck dissection in a prospective manner. Certainly, the gold standard for a prospective study is performed in a randomized, controlled setting. The Brazilian Head and Neck Cancer Group published a study with these characteristics in 1998, comparing 148 patients with T2-T4, N0 squamous cell carcinoma of the oral cavity, randomized to either MRND with accessory nerve preservation or supraomo- hyoid dissection.11 They found no differences in locoregional recurrence or survival, but the modified radical neck group had a significantly higher complication rate (41% MRND vs. 25% supraomohyoid). Complications observed included flap necrosis, wound infection, fistula, vascular rupture, hematoma, seroma, chyle leak, and postoperative death. All patients with positive nodes received postoperative radiation, and four patients with clinically positive nodes were converted to MRND at the time of the initial surgery, but were still included in the cohort. This study has often been cited to confirm the oncological equivalence of supraomohyoid neck dissection to MRND in the treatment of oral cavity cancer.
9.2 Functional Outcomes
Supraomohyoid neck dissection anatomically preserves the sternocleidomastoid muscle, internal jugular vein, and the spinal accessory nerve, and significantly limits the caudal extent of the dissection. The benefits of this approach may appear obvious to the surgeon, but systematic measurement has been difficult, as the preservation of these structures may not have a direct correlate in function, or quality of life (QOL). In these regards, Goldstein et al performed a review on articles looking at shoulder dysfunction after neck dissection. Their exhaustive review highlights the difficulty in characterizing and measuring shoulder dysfunction and surgical extent. Most articles agree, though, that there is an improvement in shoulder dysfunction in selective (compared to radical) neck dissections and that any manipulation of the accessory nerve can result in a degree of dysfunction.12 Similarly, the benefits of supraomohyoid neck dissection on QOL were confirmed in a large European study including patients from Sweden, Germany, Austria, and Switzer- land.13 This retrospective study involved 1,652 patients with oral squamous cell carcinoma, who completed a QOL questionnaire at least 6 months after surgery. Overall, patients with supraomohyoid neck dissection had significantly improved scores for neck mobility and shoulder and arm movement when compared to those who underwent a modified or radical neck dissection.
Oral cavity cancer is unique in the head and neck area due to its high incidence of occult nodal metastases, defined as a cN0 but microscopically positive lymph nodes. That is to say, physical examination of the neck does not reveal any concerning lym- phadenopathy, and nor does imaging, but histopathologic assessment reveals metastatic carcinoma in at least one lymph node. Given the lymphatic drainage pattern of the oral cavity, a supraomohyoid neck dissection will address the neck levels at highest risk of harboring occult nodal disease. Therefore, a supraomohyoid neck dissection for N0 oral cavity disease is considered both diagnostic and therapeutic. Some have posited if observation of N0 necks may be substituted for supraomo- hyoid neck dissection, and multiple studies have attempted to address this question. In this regard, a recent meta-analysis from Abu-Ghanem concluded that patients undergoing elective neck dissection had better regional- and disease-specific survival compared to those who were observed.14 While oral cavity cancers constitute the most common indication for the procedure, its indications encompass any primary location where levels I to II or III are the primary echelon for lymphatic drainage, including oropharynx, sinonasal, salivary glands, and some cutaneous malignancies. Furthermore, it is important to keep in mind that low-volume nodal disease can also be addressed with a supraomohyoid neck dissection.
9.4 Surgical Technique
The dissection begins with an incision in the neck. The incision should be designed such that it allows access to the areas of interest, but is also cosmetically acceptable. If it is possible to hide a scar in an existing skin crease, the patient will have an improved cosmetic outcome. Anteriorly, in order to reach the submental triangle, the incision can be curved upward or extended across the midline (Fig. 9.1). Remember that most radiation oncologists will radiate the entire incision as part of the postoperative radiation field; therefore, it is important to make an incision large enough to allow adequate access, but not larger than necessary. This author has not seen significant cosmetic differences in scarring in patients incised with a knife compared to the Bovie on the cut setting, particularly for those who undergo postoperative radiation. Subplatysmal flaps are raised. The external jugular vein and the greater auricular nerve should be preserved. Superior flap dissection should be performed exactly at the level of the platysma so as to not disrupt the marginal mandibular nerve. The marginal mandibular nerve is identified, traced, and preserved (Fig. 9.2). The dissection begins inferior to the submandibular gland, where the posterior belly of the digastric muscle is identified and traced anteriorly to skeletonize the anterior belly of the muscle. The fi- brofatty contents of the area between the two anterior bellies of the digastric and superficial to the mylohyoid should be removed as midline level IA neck dissection. Level IA can be transected and sent as a separate specimen. Attention is then brought back toward the submandibular gland, which is retracted inferiorly and anteriorly. The hypoglossal nerve should be identified just superior to the posterior belly of the digastric, and deep to the submandibular gland. The lateral edge of the mylohyoid muscle is skeletonized and retracted; part of the gland will wrap around the lateral edge of this muscle. The nerve to the mylohyoid is a branch of the inferior alveolar nerve and needs to be transected. As you free the submandibular gland up on its posterior surface, you will identify the lingual nerve. The lingual nerve is always superior to the hypoglossal nerve, and both nerves should be clearly identified prior to proceeding with the next steps. The submandibular ganglion of the lingual nerve is then transected. The submandibular duct will be visible and should be ligated. The facial artery and vein will be noted at the posterior aspect of the submandibular gland. The artery may be entering the submandibular gland itself, or often just sends off a large branch into the gland. The facial artery can be dissected distally to preserve as much length as possible if free flap reconstruction is anticipated. The facial nodes around the facial vein and facial artery should also be removed with the specimen. It is wise to always go back and palpate this area to ensure no lymph nodes have been left behind. This completes the level Ib dissection.
Fig. 9.1 Diagram of the most commonly used cervical incisions for a supraomohyoid neck dissection. (a) Unilateral apron approach extending to the submental area. (b) Bilateral apron incision extending across the midline. (c) Unilateral modified Schobinger incision. (d) Bilateral modified Schobinger incision.
The upper jugular nodes are then addressed. The posterior belly of the digastric muscle is exposed, and the tail of the parotid is identified at its posterior aspect. The dissection proceeds just inferior to the posterior belly of the digastric, where the tissue is divided in plane parallel to muscle to identify the jugular vein. Be cautious as there may be a large retromandibular vein joining the internal jugular vein in a “Y” configuration. The hypoglossal nerve and its associated ranine veins can also be identified in this area, as well as the ansa cervicalis descending from the hypoglossal nerve (Fig. 9.3). The dissection then proceeds laterally, toward the sternocleidomastoid muscle. The fascia of the sternocleidomastoid muscle should be incised along its anterior border. It is not necessary to resect external jugular nodes for aerodigestive tract cancers, but external jugular node dissection is indicated for cutaneous malignancies. Keeping the fascia along the anterior aspect of the sternocleidomastoid muscle intact may help prevent fibrosis, stressing the importance of incising the fascia along the anterior/medial border of the muscle. The fascia along the posteromedial aspect of the sternocleidomastoid muscle—part of the superficial layer of the deep cervical fascia—is dissected off the muscle. As we approach the posterior border of the muscle, the angle of the dissection is changed from posterior to medial, and the superficial layer of the deep cervical fascia is incised to expose the fibrofatty contents lying deep to it. These are then grasped with Allis clamps and reflected anteromedially. The upper cervical rootlets are preserved, and dissected medially, thus releasing the posterior attachments of the specimen. The spinal accessory nerve is exposed and traced toward the posterior belly of the digastric.
Fig.9.2 Boundaries for elevation of the superior subplatysmal skin flap. The marginal mandibular branch of the facial nerve can be visualized crossing the facial vessels in a superficial plane. (Netter medical illustration used with permission of Elsevier. All rights reserved.)
Most commonly, the spinal accessory nerve will course lateral to the internal jugular vein, but rarely it may “split” the vein or course medial to it. The prominence of the transverse process of C2 can routinely be palpated at this point. When searching for the spinal accessory nerve, it is important to know that a branch of the occipital artery is often within a few millimeters of the nerve, lying in a plane immediately superficial to it. This vessel can be used as a landmark to help identify the nerve, and it may be safely ligated. If level IIB are to be resected, limit the retraction and manipulation of the spinal accessory nerve as traction injury is common. The omohyoid muscle is exposed lower in the neck, and used as the inferior boundary for the dissection. The internal jugular vein can be consistently identified under the tendon of this muscle, and its lateral aspect should be exposed. There should not be any lateral branches off the internal jugular vein. The fibrofatty contents of levels II and III are reflected medially and dissected off the deep muscles of the neck, internal carotid artery, and internal jugular vein. Caution should be used to not injure the vagus nerve with the Bovie during this maneuver. This completes the level II and III neck dissection. The specimen should be divided into levels and sent separately ex vivo, to allow each lymphatic level to be examined and recorded in the pathological report.
Fig. 9.3 Intraoperative photograph of a completed supraomohyoid neck dissection. The posterior belly of the digastric muscle is retracted to show the hypoglossal nerve. Posteriorly, the spinal accessory nerve can be visualized as it enters the sternocleidomastoid muscle.
A few technical aspects of the supraomohyoid neck dissection are controversial. These include preservation of the submandibular gland, nodal yield, and the need for resection of level IIB in patients with occult oral cavity disease.
Is it absolutely necessary to remove the submandibular gland during a supraomohyoid neck dissection? The submandibular gland should of course be removed if tumor is invading directly into it. Advocates of standard removal also suggest that it is easier to address the adjacent facial nodes when the submandibular gland has been removed. Opponents to routine removal argue that—as opposed to the parotid—there are no lymph nodes within the substance of the submandibular gland. In Bocca’s landmark 1967 paper “A Conservation Technique in Radical Neck Dissection,” he proposed preserving the submandibular gland, as there is no lymphatic drainage within the gland.4 He argued that the fascial layers of the neck convolve around the gland, and hence the lymph nodes would be outside that fascia, therefore making it oncologically safe to spare the gland. The goal of submandibular gland preservation would be to maintain its salivary function in order to prevent xerostomia. Radiation therapy to any salivary gland results in loss of salivary function above 39 Gy.15 Therefore, if the primary tumor already has indications for postoperative radiation (bone or perineural invasion), and the submandibular area is going to be radiated postoperatively, it is best to resect the submandibular gland. The salivary function of the gland will be negligible after radiation therapy, and its removal will ensure that all the facial nodes are properly addressed. In addition to prevention of xerostomia, advocates of preservation also cite the incidence of marginal mandibular, hypoglossal, and lingual nerve injuries as justifications to spare the gland.16.17
The dissection of level IIB—lateral to the spinal accessory nerve—can result in symptomatic shoulder dysfunction, even if the nerve is anatomically intact. This is likely due to traction injury during dissection. In continued efforts to reduce morbidity associated with neck dissection, the need for dissection of level IIb in cN0 or low-volume nodal disease has been questioned. As it relates to oral cavity disease, the consensus seems to be that level IIB need not be dissected if level IIA is negative, with consideration for elective dissection in lateral tongue disease.18.19 Elsheikh et al examined 48 patients with oral cancer and cN0 necks, and studied the level IIb nodes, specifically looking for micrometastasis.20 They found a 10% rate of micrometastasis to the IIB nodal basin, including all oral tongue primary subsites. As such, they recommended elective dissection of level IIB for all oral tongue cancers, but not for other oral cavity sites. In terms of the oncological benefits of elective neck dissection, the best evidence comes from a landmark study by Vaish et al.21 They prospectively studied patients with early oral cavity cancer with cN0 necks. Patients were randomized to elective neck dissection versus observation with a therapeutic (or salvage) neck dissection if regional metastasis developed. Patients with upfront elective neck dissection had improved survival compared to those who underwent a therapeutic (salvage) neck dissection.
The yield of lymph nodes has been studied as a guide to help define an oncologically complete supraomohyoid neck dissection. Pou et al found a significantly higher rate of positive nodes in specimens that contained more than 18 nodes (36 vs. 15%) and suggested further study.22 It is always best practice to review the pathological report to determine the number of nodes removed; any specimen containing less than 10 lymph nodes is suggestive of an incomplete dissection. In this regard, the practice of “berry picking” lymph nodes is strongly discouraged, and every effort should be made to perform a standardized, compartment-oriented dissection of the neck levels to be addressed.
In conclusion, the supraomohyoid neck dissection is considered by many as the standard of care for cN0 or low-volume oral cavity cancer. When compared to the radical neck dissection, or MRND, this procedure yields similar oncologic outcomes but improved functional status.
 Patel KN, Shah JP. Neck dissection: past, present, future. Surg Oncol Clin N Am. 2005; 14(3):461-477, vi
 Crile G. Landmark article Dec 1, 1906: excision of cancer of the head and neck. With special reference to the plan of dissection based on one hundred and thirty-two operations. By George Crile. JAMA. 1987; 258(22):3286-3293
 Ward GE, Robben JO. A composite operation for radical neck dissection and removal of cancer of the mouth. Cancer. 1951; 4(1):98-109
 Bocca E, Pignataro O. A conservation technique in radical neck dissection. Ann Otol Rhinol Laryngol. 1967; 76(5):975-987
 Suarez O. El problema de las metastasis linfâticas y alejadas del cancer de lar- inge e hipofaringe. RevOtorrinolaringol. 1963; 23:83-99
 Ferlito A, Rinaldo A. Osvaldo Suârez: often-forgotten father of functional neck dissection (in the non-Spanish-speaking literature). Laryngoscope. 2004; 114 (7):1177-1178
 Lindberg R. Distribution of cervical lymph node metastases from squamous cell carcinoma of the upper respiratory and digestive tracts. Cancer. 1972; 29 (6):1446-1449
 Byers RM, Wolf PF, Ballantyne AJ. Rationale for elective modified neck dissection. Head Neck Surg. 1988; 10(3):160-167
 Medina JE, Byers RM. Supraomohyoid neck dissection: rationale, indications, and surgical technique. Head Neck. 1989; 11(2):111—122
 Spiro JD, Spiro RH, Shah JP, Sessions RB, Strong EW. Critical assessment of supraomohyoid neck dissection. Am J Surg. 1988; 156(4):286—289
 Brazilian Head and Neck Cancer Study Group. Results of a prospective trial on elective modified radical classical versus supraomohyoid neck dissection in the management of oral squamous carcinoma. AmJ Surg. 1998; 176(5):422—427
 Goldstein DP, Ringash J, Bissada E, et al. Scoping review of the literature on shoulder impairments and disability after neck dissection. Head Neck. 2014; 36(2):299—308
 Spalthoff S, Zimmerer R, Jehn P, Gellrich NC, Handschel J, Krüskemper G. Neck dissection's burden on the patient: functional and psychosocial aspects in 1,652 patients with oral squamous cell carcinomas. J Oral Maxillofac Surg. 2017; 75(4):839—849
 Abu-Ghanem S, Yehuda M, Carmel NN, et al. Elective neck dissection vs observation in early-stage squamous cell carcinoma of the oral tongue with no clinically apparent lymph node metastasis in the neck: a systematic review and meta-analysis. JAMA Otolaryngol Head Neck Surg. 2016; 142(9):857—865
 Murdoch-Kinch CA, Kim HM, Vineberg KA, Ship JA, Eisbruch A. Dose-effect relationships for the submandibular salivary glands and implications for their sparing by intensity modulated radiotherapy. Int J Radiat Oncol Biol Phys. 2008; 72(2):373—382
 Razfar A, Walvekar RR, Melkane A, Johnson JT, Myers EN. Incidence and patterns of regional metastasis in early oral squamous cell cancers: feasibility of submandibular gland preservation. Head Neck. 2009; 31(12):1619—1623
 Malgonde MS, Kumar M. Practicability of submandibular gland in squamous cell carcinomas of oral cavity. Indian J Otolaryngol Head Neck Surg. 2015; 67 suppl 1:138—140
 Lim YC, Song MH, Kim SC, Kim KM, Choi EC. Preserving level IIb lymph nodes in elective supraomohyoid neck dissection for oral cavity squamous cell carcinoma. Arch Otolaryngol Head Neck Surg. 2004; 130(9):1088—1091
 Bhattacharya A, Adwani D, Adwani N, Sharma V. Is it worthy? Removal of level IIB nodes during selective neck dissection (I-III) for oral carcinomas. Ann Maxillofac Surg. 2015; 5(1):20—25
 Elsheikh MN, Mahfouz ME, Elsheikh E. Level IIb lymph nodes metastasis in elective supraomohyoid neck dissection for oral cavity squamous cell carcinoma: a molecular-based study. Laryngoscope. 2005; 115(9):1636—1640
 Vaish R, Gupta S, D'Cruz AK. Elective versus therapeutic neck dissection in oral cancer. N EnglJ Med. 2015; 373(25):2477
 Pou JD, Barton BM, Lawlor CM, Frederick CH, Moore BA, Hasney CP. Minimum lymph node yield in elective level I-III neck dissection. Laryngoscope. 2017; 127(9):2070—2073