Axial CT shows two enlarged nodes on the left at level II. The nodes are rounded, and there is central necrosis. The nodes appear fused and fixed to the sternocleidomastoid muscle
Axial cut fused PET/CT shows node with increased SUV on the right side adjacent to the external thyroid cartilage of the larynx
A number of studies in the last 10 years have shown that PET scans in N0 necks cannot be used to define surgical management due to a limited sensitivity for small deposits and a relatively high number of false positives [13, 14]. These findings have not changed in recent published work with research in 2012 showing PET/CT having a much reduced rate of efficiency for N0 necks as opposed to N+ necks and concluding that it has little advantage in staging N0 necks . PET/MR seems to have no advantage over PET/CT .
In comparing different imaging techniques, conclusions are somewhat varied. One 2014 prospective study examined patients deemed N0 by CT and/or MR who were then examined with ultrasound (US) and found that the number of patients with undiagnosed occult metastases decreased from 31 to 16 %, while 6 % of patients were over-staged by US . In another study using multiple studies, it was concluded that fusion of (18)F-FDG-PET/MRI and (18)F-FDG-MRI plus DWI (diffusion-weighted imaging) may not increase nodal detection and N staging in oral cancer compared to US and (18) F-FDG-PET/CT . Chaukar et al. found contrast-enhanced CT to give better concordance with histology in the N0 neck than either US or PET/CT .
In 2012 a meta-analysis comparing imaging modalities for the N0 neck identified 168 articles of which 7 studies fulfilled the inclusion criteria for CT, 6 studies for MR, 11 studies for PET, and 8 studies for US. The study conclusion was “modern imaging modalities offer similar diagnostic accuracy to define and diagnose clinically N0 neck.” However, they could only state that avoiding elective neck dissection was acceptable in certain select cases . In clinical practice, it appears that CT scan is most likely to be the initial study chosen for the N0 neck , despite the fact that “diagnostic accuracy of CT is limited among N0 oral cavity SCC patients” .
Although imaging has not provided an answer to diagnosis and staging of the N0 neck, there is evidence that it may provide prognostic information regarding outcomes. Joo et al. in 2013 showed that SUV max in PET/CT scanning was raised in lymph nodes with extracapsular spread; the ability to detect ECS also allowed prediction of 5-year worse survival . The same authors also found a correlation between resection margin involvement and an SUV >8.5 to be associated with adverse outcome . Other authors have found SUV (mean) increase in the primary tumor to predict inferior disease-free survival . In addition to raised SUV, metabolic tumor volume (MTV) as measured on PET has been found to be a significant prognostic factor for disease recurrence and mortality , as well as disease-free and overall survival .
Another area where PET has proved superior in neck evaluation is in recurrent regional disease. Lee et al. found that sensitivity and NPV for PET scan for recurrence was 92.5 % and 94.8 %, respectively, compared to 55 % and 76.9 % for CT scan. They recommend PET scan for routine surveillance . PET/CT was also found to be superior to CT/MRI in detecting residual nodal disease in patients undergoing salvage surgery allowing better preoperative diagnosis .
US-guided fine needle aspiration biopsy (FNAB) has been shown to be very accurate in diagnosing lymph node status of the neck. Battenburg de Jong et al.  reported sensitivity of 98 % and specificity of 95 %, while Van de Brekel published a 96 % success rate in aspirating nodes >5 mm in diameter . A 2012 prospective study compared CT, PET/CT, and US-guided FNAB to the final pathology obtained by neck dissection. Although US-guided FNAB showed the highest correlation with exact N classification and the smallest number of over-staged patients, it was concluded that none of the three modalities was reliable enough to replace neck dissection in N0 necks .
In addition to being used for diagnosis, FNAB has been used to guide therapy by assessing immunocytochemical profiles of cells to predict radiation response  and more recently to assess p16 status in possible HPV-associated head and neck cancers. HPV status can not only be useful in allowing de-escalating of therapy, but in nodes with an unknown primary, it may guide radiation fields to the oropharyngeal region reducing wide field radiation.
It is still felt by most head and neck surgeons that open biopsy of a neck node will compromise subsequent treatment and reduce outcomes , although Parsons et al. in 1985 showed that excisional removal of the entire node followed by radiation therapy gave a 96 % control of neck disease and a 75 % disease-free survival . His work also demonstrated that incisional biopsy led to very poor outcomes.
7.4 The N0 Neck
It can be seen from the above literature review that current clinical, imaging and FNAB techniques are not sufficiently accurate enough to diagnose occult disease (micrometastasis) in the N0 neck. The question becomes whether to treat the neck or observe and if we decide to treat then whether to give radiation therapy or elective neck dissection. As either treatment modality is associated with morbidity then clearly there must be a benefit to the patient as opposed to just observing. There are four randomized controlled trials in the literature which have examined survival in early oral cancer patients with N0 necks treated either with elective neck dissection or observation. The first two trials were undertaken in France  and India  in the 1980s both with approximately 70 patients and oral tongue cancers. Neither trial demonstrated a significant survival benefit for neck dissection although there was a trend toward improved survival in tumors deeper than 4 mm in the Indian study. In 1994 Kligerman et al. published their trial of 67 patients with T1-2 N0 carcinomas of the tongue/floor of mouth and showed that disease-free survival rates at 3.5 years were 49 % for the observation and 72 % for the elective neck dissection cohort. The study also stratified patients into those with tumors >4 mm or <4 mm. Results demonstrated that stage II (T2) and >4 mm thick tumors were significantly associated with treatment failures. The trial concluded that neck dissection was mandatory in early stage oral SCC because of better survival than resection of the primary alone with observation of the neck and the poor salvage rates for neck relapse. This trial also provided the evidence for an elective SOHND approach to the N0 neck which remains the standard of care . It is important, however, to appreciate that the 2009 prospective randomized trial by Yeun et al. failed to show any survival advantage for elective neck dissection .
Why should this early occult disease impact survival? One explanation is that ECS can occur at an early stage with very small deposits. Two large retrospective studies of 300 and 103 elective neck dissections for N0 disease showed similar rates of positive nodes 33 and 34 %, with rates of ECS of 24 and 49 %. ECS impacted rates of recurrence and disease-free survival [40, 41]. Another reason is that despite close observation patients tend to be diagnosed at a late stage rarely with N1 disease . This may also be the reason why Yeun et al. in an initial retrospective study found salvage surgery for recurrence in “observed” necks to have poor outcomes . However, even metastasis so small that were only detected by IHS or QRT-PCR can affect recurrence and/or survival [44, 45]. Primarily because of Kligerman et al.’s study  elective SOHND neck dissection became the standard of care for the “at-risk” N0 neck.
As evidence showed only approximately 33 % of elective neck dissections for N0 disease, it was not obvious which patients with oral cancer and N0 neck disease were at most risk for occult regional disease. Again from Kligerman et al.’s study , it appeared that patients having T2 tumors with thickness of 4 mm or greater had significantly lower survival. The initial studies on tumor thickness in SCC of the oral cavity being correlated with lymph node metastases were published in 1981 [46, 47]. Using the technique of decision analysis, Weiss et al. proposed that any patient with a risk above 20 % should undergo selective neck dissection . This 20 % guideline covered all T2-4 tumors of the oral cavity plus any T1 tumors thicker than 4 mm.
Controversy has been generated over whether level IIB nodes or level IV nodes require to be removed in SOHND for an oral cavity primary and whether the neck dissection should be in-continuity or discontinuity with resection of the primary tumor. Regarding level IIB, the incidence of nodal involvement in the N0 neck is 6 % for all SOHNDs [49, 50] but is as high as 18 % in positive SOHND . In a prospective study of 74 patients with oral cancer the occult positivity in the neck was 32 % (only 5 % of nodes at level IIB). In the final histopathologic examination of the neck dissection specimens, patients with positive nodes at level IIB all also had positive nodes at level IIA. In oral SCC the dissection of level IIB nodes is therefore not essential unless other palpable positive nodes at level IIA are discovered intraoperatively; this is important as dissection of level IIB is associated with some accessory nerve morbidity.
In 1997 Byers et al. advocated adding level IV dissection to the SOHND in cases of oral tongue cancer. His argument was based on retrospective data which showed a high level of “skip metastases” for oral tongue with 15.8 % of his series showing only level III or IV involvement  (Fig. 7.3). This conclusion was not upheld by a prospective trial which found an incidence of level IV nodes to be 4 % for oral tongue cancer and recommended only dissection of levels I–III . The argument for in-continuity dissection revolves around the potential for missing important lymphatic tissue or nodes if a separate glossectomy and SOHND are performed with consequent higher recurrence rates. In one study, patients with discontinuous dissection had a 63 % 5-year survival compared to 80 % for patients where the primary resection and neck dissection was carried out in-continuity . However, the in-continuity approach does sacrifice more normal tissue and creates an open tract between the mouth and neck leading to a greater potential for complications. A large Brazilian study with 193 patients showed no difference in disease-free or disease-specific survival associated with in-continuity versus discontinuity resections . At the current time in the USA, discontinuous dissection appears to be the standard of care. This approach will miss removing sublingual lymph nodes which are rare but are reported to occasionally be the first echelon nodes for oral tongue cancer .
(a, b) Coronal and sagittal PET shows primary tongue cancer with “skip” metastasis to level III
In patients who are medically unfit or refuse surgery with N0 neck at high risk of occult disease, there is good evidence that 50 Gy of radiation can effectively sterilize the neck [56, 57]. Indeed as long ago as 1972, Fletcher compared 187 cases with no elective irradiation to 187 cases with elective irradiation to the N0 contralateral neck and showed the incidence of delayed nodes to be 24 % and 3 %, respectively . However, as most oral cancers are primarily dealt with surgically, it seems to make sense to undertake elective neck dissection in high-risk patients at the same time, as well as the staging information that is obtained. The argument can be made that patients with subclinically positive disease with ECS who only receive elective radiation do not get the benefit of chemoradiation which is indicated for ECS and that staging the neck by elective neck dissection can more accurately define the need for and type of adjuvant therapy. In the future sentinel node, biopsy may become the method of choice for staging the N0 neck, and this subject is addressed in another chapter.
7.4.2 Surgical Technique
The author uses a similar approach to SOHND as that reported by Medina and Byers  as he has previously described  (Fig. 7.4). The initial incision is made from the mastoid to the midline of the neck, placed in a mid-neck skin crease. The flaps are raised in a sub-platysmal plane from the area where the omohyoid muscle crosses the internal jugular vein (IJV) to the lower border of the mandible. The fascia is raised off the sternocleidomastoid muscle (SCM) over its anterior border and deep to the muscle. The posterior belly of the digastric muscle is identified deep to the SCM and close to the mastoid. Dissection of the fat beneath the inferior border of the digastric will identify the proximal end of the IJV and the accessory nerve as it crosses the posterior IJV at the level of the atlas vertebra. If there are no palpable hard nodes at level IIA, the level IIB triangle will not be dissected. The fatty tissue at the apex of the triangle between the accessory nerve and IJV is dissected down to the prevertebral fascia. This fat is mobilized from the accessory nerve and the posterior border of the IJV. Dissection continuous inferiorly releasing the fat from the SCM posteriorly and the IJV anteriorly till the omohyoid muscle superior border is seen. Care is taken to leave the nerves of the deep cervical plexus intact.
The completed SOHND. The sternocleidomastoid muscle is retracted with an army-navy retractor. The long arrow crosses the carotid and IJV and points to the accessory nerve
The fatty tissue is mobilized anteriorly to the IJV by dissecting the fascia off the IJV. Dissection continues anterosuperior in the anterior triangle of the neck with the anterior belly of the omohyoid delineating its anterior extent. Once the anterior belly of the digastric is identified, level I will be dissected. If the level IA nodes are to be removed (submental), this will be done starting from the contralateral anterior belly of the digastric muscle and mobilizing the fat and adipose tissue to the ipsilateral submandibular triangle. The mandibular branch of the facial nerve is identified by careful dissection below the mandible and mobilized cephalad superior to the lower border of the mandible. The common facial vein and facial artery are tied off at the lower border (unless they are to be used for free flap reconstruction). The level IB fat and nodes including the submandibular gland are mobilized off the mylohyoid muscle identifying the posterior border of that muscle as dissection proceed posteriorly toward the mandibular angle. A vein retractor is used to retract the mylohyoid muscle anteriorly to identify the lingual nerve. The branch from the lingual nerve to the submandibular gland is clipped and cut, and Wharton duct is clipped and cut. The specimen is now pedicled on the proximal trunk of the facial artery as it emerges from deep to the posterior belly of the digastric muscle to pass superiorly to the muscle. This is doubly ligated and cut and the specimen removed. The platysma and skin are closed in two layers. Large round suction drains are placed prior to closure.
The specimen is oriented and pinned on a cork board with a diagram for the pathologist.
7.4.3 Adjuvant Therapy
It is currently a standard of care to examine histopathologic data at multidisciplinary tumor boards. Adjuvant therapy is usually recommended based on the current NCCN guidelines . The guidelines for adjuvant therapy in the postoperative neck at are based upon two large prospective, randomized trials (RTOG 9501 in the USA and EORTC 22931 in Europe) comparing postoperative radiation to postoperative chemoradiation in patients at high risk for locoregional relapse [62, 63]. Long-term follow-up of the cohorts of these two trials have served to refine the criteria for the use of both radiation and chemo/radiation [64–66]. Current recommendations recommend no adjuvant therapy if the neck dissection is N0 or N1 histopathologically without extracapsular spread. Any N2 neck or greater histopathologically will be recommended for adjuvant radiotherapy if there is no ECS. If there is ECS in any neck dissection, then chemo/radiation is recommended.
7.5 The N-positive Neck
The neck with clinically positive nodes was treated by radical neck dissection based upon Crile’s classic description in 1906 . The radical neck dissection (RND) encompassed levels I–V with the removal of the SCM, IJV, and spinal accessory nerve. The removal of these three structures especially the accessory nerve did lead to a significant morbidity for patients, and modified radical neck dissections (MRND) were developed that still allowed complete dissection of levels I–V while sparing one or more of the SCM, IJV, and spinal accessory nerve. Lingeman et al. studied outcomes of patients who underwent either RND or MRND, finding that regional recurrence rates for N0, N1, and N2 necks were 14, 15, and 26 % in patients who had RND and 0, 16, and 25 % for MRND patients . The MRND was demonstrated to be oncologically safe for N0 and N1 necks [69, 70], and it was also shown that the spinal accessory nerve could usually be safely preserved even with advanced neck disease, ECS and nodes along its course unless directly invaded by tumor . Between 1984 and 1990, there was much discussion whether the N1 neck could be safely treated by SOHND , whether selective neck dissection levels I–IV  was required or whether MRND was essential . In view of Shah’s earlier study which showed an incidence of 20 % level IV nodes in the N-positive neck , it appears that at least a selective neck levels I–IV or MRND is essential. Other recent studies confirm this data and emphasize that positive nodes at level IIA are a predictor for positivity at both levels IV and IIB .
More recent studies have looked at outcomes for selective neck dissection for clinical N1 neck disease. Pellitteri et al. found that for pathologic N0, 1 of 33 patients (3 %) recurred in the neck, and for proven N1 disease, 1 of 8 patients (12.5 %) recurred. They felt selective neck dissection was suitable for the N1 neck, provided radiation was given for patients with N2 disease or ECS . In another study of SOHND for N-positive necks, regional control was 88 % for N0 necks and 71 % for N-positive necks, and this was significantly improved by radiation therapy for the N-positive group . Control rates in the SOHND cases with positive nodes who were irradiated were comparable to those patients with level I–V neck dissections and radiation. Further studies have confirmed these results using a variety of different selective neck dissections, showing comparable outcomes to MRND and RND provided radiation was given for greater than N1 disease and chemo/radiation for ECS [78–80]. It is difficult to assess whether SOHND is adequate as a selective neck dissection for the N-positive neck as many of these studies used a variety of selective neck dissections. In Givi et al.’s paper, 80 % of their selective neck dissections included level IV which they felt was particularly indicated for oral cavity primaries . As MRND has more morbidity than selective neck dissection , level V nodes should only be removed when they are at high risk due to clinically evident ECS, multiple LN involvement and cN1 with deep jugular chain of LN involvement . The IJV is usually retained in selective neck dissection especially if microvascular reconstruction is required; however, there are some studies that show an increased rate of neck failure with preservation of the IJV .
In concluding recommendations for the N-positive neck for an oral cancer primary, it appears that for the clinically N1 neck, a selective neck dissection levels I–IV or an MRND can be used. If the neck is found to be N2 or greater histopathologically, then adjuvant radiation is indicated, while for ECS chemo/radiation should be given. In countries where cost is a major driver of health care, MRND may be a more cost-effective choice . In the clinically N2- or N3-positive neck, then MRND or RND is the method of choice. The accessory nerve can usually be spared except in extensive disease , and all cases will have adjuvant radiation with chemo/radiation used for ECS. Prognosis is poor in advanced neck disease with multiple nodes and ECS, and approximately 50 % of these patients will develop distant metastases, most frequently to the lung. Whether contralateral neck dissection is indicated has been debated but the rate of contralateral neck disease is only around 4 % , and the majority of patients will receive radiation to the contralateral neck as part of their adjuvant regime. Nodal disease <3 cm is well controlled by radiation therapy, and any microscopic disease in the contralateral neck should be sterilized with 50 Gy of radiation.
7.5.2 Surgical Technique
The author’s preferred methods for RND  and MRND  are published in the literature. The author prefers a MacFee incision (Fig. 7.5), for all level I–V dissections to prevent trifurcation breakdown and carotid blowout (Fig. 7.6). If the sternocleidomastoid muscle is to be kept in MRND, then a wine glass (Schobinger) incision is usually safe. The skin flaps are raised in a sub-platysmal plane (if ECS involves platysma or skin, it will of course be sacrificed). The author begins the dissection posteriorly finding the anterior belly of the trapezius muscle 1 cm above the clavicle and defining this structure as the posterior limit of the dissection. The accessory nerve is identified as it passes beneath the trapezius 2–4 cm above the clavicle, in an RND this will be sacrificed in an MRND usually dissected and preserved. The supraclavicular fat and nodes are mobilized off the prevertebral fascia taking care not to damage branches of the brachial plexus. The location of the brachial plexus is at the point where the omohyoid muscle passes under the clavicle. The omohyoid is sacrificed in the RND but may be retained in the MRND. The sternocleidomastoid muscle is divided off the clavicle and sternum and dissected cephalad. The remaining supraclavicular fat is mobilized off the prevertebral fascia and mobilized cephalad. The transverse cervical artery and vein runs about 2 cm above the clavicle and may be preserved; it lies superficial to the phrenic nerve as it crosses the anterior scalene muscle. Care should be taken when mobilizing the level IV fat/nodes close to the IJV on the left side not to damage the thoracic duct (Fig. 7.7). At this point the IJV is identified in the base of the neck. If it is to be sacrificed and ligated, care is taken to separate its deep surface from the vagus nerve. The block of tissue fat with IJV and sternocleidomastoid muscle are now dissected superiorly along the prevertebral fascia sacrificing the large cervical nerve branches of the phrenic nerve (C 3, 4 and 5) as they pass into the specimen. In the RND this is a quick and easy dissection to the level II area. At this point the sternocleidomastoid muscle is sectioned off the mastoid from the apex of the posterior triangle. Then following a line from the tip of the mastoid to the angle of the mandible, the sternocleidomastoid is sectioned superiorly along with the tail of the parotid to the depth of the underlying posterior belly of digastric muscle. The superior end of the accessory nerve is identified and cut and the superior portion of the IJV ligated and cut at the level of the digastric. The specimen is mobilized forward to level I, and dissection proceeds as described for the SOND.
MacFee incision for a MRND note the bi-pedicled skin flap (large arrow). Patient has had an in-continuity resection of the left tongue/hemi-mandible and MRND
(a, b) Angiogram demonstrates pseudo-aneurysm of common carotid artery following a premonitory bleed during radiation therapy. Carotid pseudoaneurysm (arrow)
The bi-pedicled portion of the MacFee incision is retracted cephalad. The accessory nerve, sternocleidomastoid, and IJV have been sacrificed. The arrow points to the phrenic nerve. The common carotid is retracted medially
In the case of the MRND, dissection is more complex. If the accessory nerve is to be retained, it is dissected to its entry beneath the sternocleidomastoid muscle and mobilized from the underlying fat. The fat at the apex of the posterior triangle which lies superiorly (cephalad) to the nerve is mobilized from the prevertebral fascia and passed deep to the nerve to remain in continuity with the level V fat (Figs. 7.8 and 7.9). At this point if the sternocleidomastoid muscle is to be preserved, its fascia at the posterior border is raised and dissected to allow a tunnel to be created under the muscle to pass the contents from level IV and V to be passed anterior to the sternocleidomastoid into level III. Usually the author leaves the contents of levels IV and V in the posterior neck and completes the SOHND as already described (above) but leaving level III attached to level IV fat. When this is finished, it is easier to pass the contents from the posterior neck (levels IV and V) in-continuity with the SOHND, although there are usually a few irritating attachments that need to be sectioned to mobilize the specimen easily.
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