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(Radiology. 2001;218:289-293.)
© RSNA, 2001

Technical Developments

Head and Neck Squamous Cell Carcinoma: US-guided Fine-Needle Aspiration of Sentinel Lymph Nodes for Improved Staging—Initial Experience1

David R. Colnot, MD, Eline J. C. Nieuwenhuis, MD, Michiel W. M. van den Brekel, MD, PhD, Rik Pijpers, MD, PhD, Ruud H. Brakenhoff, PhD, Gordon B. Snow, MD, PhD and Jonas A. Castelijns, MD, PhD

1 From the Departments of Otolaryngology/Head and Neck Surgery (D.R.C., E.J.C.N., M.W.M.v.d.B., R.H.B., G.B.S.), Radiology (J.A.C.), and Nuclear Medicine (R.P.), University Hospital Vrije Universiteit, De Boelelaan 1117, PO Box 7057, 1007 MB Amsterdam, the Netherlands. Received November 18, 1999; revision requested December 21; final revision received March 30, 2000; accepted April 4. Address correspondence to M.W.M.v.d.B. (e-mail: kno@azvu.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
Ultrasonography (US)-guided fine-needle aspiration with cytologic examination was combined with lymphoscintigraphy for the identification of sentinel lymph nodes (SLNs) in 12 patients with a squamous cell carcinoma of the oral cavity or oropharynx. Dynamic lymphoscintigraphy and a hand-held gamma probe were used to depict the SLNs to be aspirated. Cytologic examination of the aspirated SLNs revealed neck lymph node status in patients who underwent neck dissection (n = 6). In patients who underwent only transoral excision, one false-negative cytologic result was observed. This combined approach is expected to improve the detection of occult neck lymph node metastases.

Index terms: Head and neck neoplasms, diagnosis, 262.1262, 262.3751 • Head and neck neoplasms, radionuclide studies, 262.1262, 262.343 • Head and neck neoplasms, staging, 262.1262 • Lymphatic system, neoplasms, 997.1262, 997.12985 • Lymphatic system, radionuclide studies, 997.12961 • Ultrasound (US), guidance, 997.12985


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
 Results
 Discussion
 REFERENCES
 
In patients with head and neck squamous cell carcinoma, a clinically negative neck (N0) is at risk of harboring occult metastases and is, therefore, treated electively with surgery or with radiation therapy if this risk is estimated to be higher than 20% (1). Elective neck dissection causes overtreatment for the majority of these patients, while no unequivocal advantage in survival has been demonstrated when it is compared with delayed neck dissection for patients with metastases in the neck (2,3). Transoral excision of relatively small (T1 or T2) primary tumors of the oral cavity or oropharynx, followed by a wait-and-see approach with frequent ultrasonography (US) and US-guided fine-needle aspiration with cytologic examination, may be justified to prevent elective neck dissection in these patients (4).

Because cytologic criteria are more reliable than radiologic criteria, US-guided fine-needle aspiration with cytologic examination was found to be more accurate than US, computed tomography, or magnetic resonance imaging (5). The sensitivity of US-guided fine-needle aspiration with cytologic examination for the clinically negative neck (N0) has been reported to be 44%–73%, depending on, among other things, the experience of the ultrasonographer (6–8). Since false-positive cytologic findings with lymph node aspirates are rare, specificity of US-guided fine-needle aspiration is often 100%. Inaccurate results at US-guided fine-needle aspiration and cytologic examination are thus attributed to an absence of enlarged lymph nodes, aspiration of the wrong lymph node, failure of cytologic analysis due to the presence of few tumor cells, or the presence of micrometastases in parts of the lymph nodes not aspirated (sampling error). The selection of lymph nodes to be aspirated is not easy and is based on known patterns of lymphatic spread (9) and on lymph node size and morphology as assessed with US (8). However, assessment on the basis of drainage patterns and US morphology is prone to errors, and a functional technique to identify the lymph nodes at risk of harboring an occult metastasis could improve the accuracy and reliability of cancer staging in the neck in these patients.

The concept of the sentinel lymph node (SLN) is based on the orderly progression of tumor cells within the lymphatic system. Lymph flow mapping from the tumor site to the regional lymphatic drainage area can be used to identify the primary draining lymph node (ie, the SLN) that will be the first to receive metastatic tumor cells. Radiolabeled pharmaceuticals can be injected next to the tumor, and a hand-held gamma probe is used to depict radioactive lymph nodes. Biopsy of the SLN has shown to be useful as an accurate staging technique in studies (10–12) with large series of patients with breast cancer and melanoma in which histopathologic analysis of the sampled SLN was used to accurately predict the regional lymph node status in 97%–99% of patients. Patients with a disease-free SLN may therefore be spared elective regional lymph node dissection, which would reduce morbidity in a large number of patients. With head and neck cancer, there is limited experience in gamma probe–guided SLN biopsy (13,14). To our knowledge, a combined SLN procedure with US-guided fine-needle aspiration with cytologic examination has not been performed. This approach is more attractive than biopsy since it is minimally invasive.

The purpose of our pilot study was to evaluate the feasibility of combining an SLN procedure with US-guided fine-needle aspiration and cytologic examination.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
From June 1998 to December 1998, 12 consecutive patients (nine men, three women) with a clinically negative neck (N0) assessed at palpation, a histologically proved squamous cell carcinoma of the oral cavity or oropharynx, and scheduled transoral excision or combined tumor excision with unilateral neck dissection were included in this study. The protocol was approved by the institutional medical ethics committee, and informed consent was obtained from all patients after explanation of the procedure.

Depending on accessibility of the primary tumor, three or four submucosal peritumoral injections of technetium 99m–labeled colloidal albumin (Nanocoll, Sorin Biomedica, Sallugia, Italy; particle size, 3–80 nm; total content, 40–70 MBq) in aliquots of 0.2 mL of saline were administered by using a 25-gauge needle (Fig 1). Immediately after injection, lateral dynamic scintigraphy (20 60-second acquisitions in a 128 x 128 matrix) was performed by using a gamma camera with a large field of view equipped with low-energy parallel-hole collimators (Dual Head Genesys Imaging System; ADAC Laboratories, Milpitas, Calif).



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  		Figure 1. Patient 11. Peritumoral injection of 99mTc-labeled colloidal albumin in the submucosa immediately dorsal to a primary tumor (T) on left side of the tongue.

 
The dynamic studies were followed by static scintigraphy (120 seconds) in anterior and lateral projections to avoid superimposition caused by radioactive scatter originating from the injection site over radiolabeled lymph nodes in the neck. If no SLN was depicted, additional static scintigraphy was performed after 20 or 40 minutes. After the SLN was detected, its location was marked on the skin and confirmed by a nuclear medicine physician (R.P.) using a hand-held gamma probe (CTC 4; RMD, Watertown, Mass). This gamma probe with a 14-mm diameter uses a cadmium telluride semiconductor and has a weight of 265 g, including a tungsten shield. The threshold was set between 120 and 160 keV.

Within 1 hour, lymph nodes were identified at US (7.5-MHz linear-array transducer; Acuson, Mountain View, Calif), and fine-needle aspirates were obtained for cytologic examination of the SLN, additional radiolabeled lymph nodes, and other lymph nodes on the basis of US size criteria. US-guided fine-needle aspiration was performed by one radiologist (J.A.C.) using a syringe holder (Cameco, Taeby, Sweden) and a 0.6 x 25.0-mm needle. The location of the SLN was recorded per side and level according to the Memorial Sloan-Kettering Cancer Center classification (15) (Fig 2). After preparation of the cytologic smears, residues of the aspirates from the SLN, additional radiolabeled lymph nodes, and other lymph nodes were rinsed in phosphate-buffered saline and counted in a liquid scintillation counter (Wallac, Turku, Finland) to confirm correct aspiration.



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  		Figure 2. Drawing shows lymph node levels of the neck. Level 1 includes the submental and submandibular region. Levels 2, 3, and 4 correspond to the lymph nodes of the jugular chain (ie, high-, mid-, and low-jugular, respectively). Lymph nodes in the posterior triangle and supraclavicular region are located in level 5. Level 6 corresponds to the juxtavisceral lymph nodes.

 
Patients with a primary tumor staged T3 (three patients) or T4 (two patients) underwent planned unilateral elective neck dissection the next day, which enabled evaluation of the neck dissection specimen. The hand-held gamma probe was then used to retrieve all radioactive lymph nodes from the neck dissection specimen for separate histopathologic examination. A probe count of less than 10% of the most radioactive lymph node was regarded as background. Histopathologic results of the identified SLN were compared with the cytologic results.

All seven patients with T1 or T2 stage tumors were initially scheduled for transoral excision of the primary tumor and a wait-and-see approach with strict follow-up of the neck, including palpation, US, and US-guided fine-needle aspiration with cytologic examination according to the policy of our department (4). In these patients, verification from the neck dissection specimen could not be obtained, and, therefore, the outcome of the clinical follow-up was used to evaluate the SLN concept in these patients.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
Discussion
 REFERENCES
 
At dynamic lymphoscintigraphy (Figs 3, 4), at least one radiolabeled lymph node was identified after administration of 99mTc-labeled colloidal albumin in all but one patient (Table 1, patient 5). In this patient, no focal accumulation of radioactivity was visualized, but two level I lymph nodes that were aspirated on the basis of size criteria contained radioactivity and thus were identified afterward by means of liquid scintillation counting of the aspirates. Because of its location close to the injection site, scintigraphic visualization of the SLN in this patient was most likely disturbed by radioactive scatter originating from the injection site in the floor of the mouth. In another patient, the SLN was located in level I (Table 1, patient 2), whereas in all other patients, scintigraphy showed the SLN in levels II and III. Subsequent independent localization with the hand-held gamma probe in a patient with a carcinoma in the floor of the mouth was feasible if the SLN was located in level II or lower.



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  		Figure 3a. Patient 11. (a) Left lateral dynamic lymphoscintigram obtained at 2 minutes after peritumoral injection of 99mTc-labeled colloidal albumin shows early transport of the tracer in a lymph vessel (arrow), without focal activity. (b) Left lateral static scintigram obtained at 20 minutes after injection shows two radiolabeled lymph nodes (short arrows) and a faint secondary focus (long arrow) above both lymph nodes, which represents spill of the radioactive tracer to a second-echelon lymph node. Fine-needle aspiration and cytologic findings of both radiolabeled lymph nodes were negative. In a and b, A = anterior, i = injection site, P = posterior.

 


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  		Figure 3b. Patient 11. (a) Left lateral dynamic lymphoscintigram obtained at 2 minutes after peritumoral injection of 99mTc-labeled colloidal albumin shows early transport of the tracer in a lymph vessel (arrow), without focal activity. (b) Left lateral static scintigram obtained at 20 minutes after injection shows two radiolabeled lymph nodes (short arrows) and a faint secondary focus (long arrow) above both lymph nodes, which represents spill of the radioactive tracer to a second-echelon lymph node. Fine-needle aspiration and cytologic findings of both radiolabeled lymph nodes were negative. In a and b, A = anterior, i = injection site, P = posterior.

 


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  		Figure 4. Patient 10. Anterior (left) and right lateral (right) projections of static scintigram. Right lateral projection shows the SLN (long arrow), which cannot be seen on the anterior projection because of superimposition, and the ballooning effect of the radioactive scatter originating from the injection site (i). A second radiolabeled lymph node is visible (short arrow). A = anterior, L = left, P = posterior, R = right.

 

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  		TABLE 1. Characteristics of Patients Undergoing SLN and Combined Transoral Excision with Unilateral Neck Dissection
 
Lymphoscintigraphy and/or scintillation counting of the aspirate was used to identify a total of 19 radiolabeled lymph nodes: In five patients, a single SLN was found, and in seven patients, additional radiolabeled lymph nodes were identified. Aspiration of a radiolabeled lymph node always revealed a positive result with the liquid scintillation counter. The mean radioactivity content of aspirate residues was 6,649 counts per minute (cpm) (range, 181–12,480 cpm). Counting of the aspirate residues of nonradioactive additional lymph nodes that were aspirated on the basis of US criteria resulted in background values (mean, 30 cpm). In one patient (Table 2, patient 9), two radiolabeled lymph nodes were considered too small for aspiration (<2 mm); therefore, a total of 17 radiolabeled lymph nodes were aspirated in 11 patients. In nine of these patients, cytologic findings were negative; in two patients, cytologic findings were positive.


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  		TABLE 2. Characteristics of Patients Undergoing Transoral Excision with Staging and Strict Follow-up with US-guided Fine Needle Aspiration Cytologic Examination
 
In all patients undergoing combined tumor excision with unilateral neck dissection (n = 6), the cytologic findings in the SLN were in agreement with the histopathologic findings in the neck dissection specimen (Table 1). On the basis of the cytologic results in the aspirated SLN, clinical treatment was changed in one patient. This patient had a tongue carcinoma initially staged T2N0 (Table 1, patient 6) and was scheduled to undergo only a transoral excision, but cytologic findings were tumor positive. The aspirate of an 11-mm SLN located in level II was positive, as well as that of two other lymph nodes (levels I and II) that were aspirated because of US size criteria. A combined transoral excision and neck dissection was performed. Histopathologic examination of the neck dissection specimen revealed six lymph node metastases, three in level I and three in level II.

The six patients undergoing transoral excision with a wait-and-see approach underwent follow-up with US-guided fine-needle aspiration with cytologic examination, with a mean follow-up of 11 months (range, 7–16 months) (Table 2). In one of these patients (Table 2, patient 7), a lymph node metastasis was diagnosed at US-guided fine-needle aspiration with cytologic examination after 4 months of follow-up after an initial negative aspiration and cytologic result of one SLN located in level II. Neck dissection was performed, and histopathologic examination of the specimen revealed a large lymph node metastasis with extranodal spread located from level II to level IV. Therefore, this case should be considered a false-negative finding with US-guided fine-needle aspiration with cytologic examination of an SLN.


   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
REFERENCES
 
The findings of this pilot study show that fine-needle aspiration with lymphoscintigraphy by using a hand-held gamma probe and US guidance is a feasible approach in the identification and characterization of lymph nodes in head and neck cancer. Moreover, aspiration of the visualized SLN can be confirmed by means of scintillation counting of the aspirate residue. However, difficulties in localization at scintigraphy or by using a hand-held gamma probe were encountered if an SLN was located in the submandibular region (level I) close to the injection site, that is, in a case of carcinoma of the floor of the mouth. In this case, the presence of radioactive scatter originating from the injection site made separate localization of radiolabeled lymph nodes by using scintigraphy or the hand-held gamma probe impossible. As a consequence, correct aspiration can then be confirmed only by means of scintillation counting of the aspirate residue.

In their study with gamma probe–directed SLN biopsy in oral carcinomas, Koch et al (13) also described this problem for one case. In our experience, when an SLN cannot be identified by using scintigraphy or the hand-held gamma probe, the ultrasonographer should focus on the submandibular and submental region. Findings in one of our cases (Table 1, patient 6) showed that even if an SLN is detected in level II, metastases in level I cannot be excluded. We are currently evaluating whether the use of shields at the injection site, digital subtraction techniques, and dynamic lymphoscintigraphy can reduce the risk of a missed radiolabeled lymph node close to the injection site.

An advantage of dynamic lymphoscintigraphy is its ability to discriminate between a true SLN and a spill to second-echelon lymph nodes (16) (Fig 3). The risk of superimposition of radiolabeled lymph nodes by the injection site can be reduced by using anterior and lateral imaging (Fig 4).

Although we have validated our findings in only a small series of patients, the cytologic findings in the SLN aspirates were used to correctly predict the regional lymph node status when combined tumor excision and neck dissection were later performed (Table 1). Of all patients treated with transoral excision of the primary tumor and a wait-and-see approach with strict follow-up of the neck, one patient developed a large lymph node metastasis 4 months after surgical treatment of the primary tumor (Table 2). Most likely, this lesion was already present at the time of primary surgery, and it was therefore considered a false-negative SLN aspiration. Since most recurrences occur within 2 years after primary treatment, a longer follow-up for this group of patients is mandatory.

As illustrated in Tables 1 and 2, the largest lymph node is not always visualized at lymphoscintigraphy. In four patients (Table 1, patient 4; Table 2, patients 8, 10, 11), the largest lymph node identified at US did not contain radiolabeled colloidal albumin. Lymphoscintigraphy thus resulted in the identification of smaller lymph nodes that would probably not have been selected for aspiration by using US criteria. This observation had no consequence for patient care, since cytologic findings were negative for all aspirated lymph nodes in these patients.

In one patient (Table 2, patient 9), two small radiolabeled lymph nodes (<2 mm) were identified by using the SLN procedure but were considered too small for fine-needle aspiration. Therefore, it could be concluded that the radioactivity attributed to these lymph nodes was determined only by the exclusion of the presence of other lymph nodes at the mark. Although the cytologic result of the aspirated SLN altered the surgical treatment in one patient (Table 1, patient 6), it seems likely that this SLN (11 mm) would also have been selected for aspiration because of US criteria.

It has been reported (12) with breast cancer that, ironically, extensive tumor infiltration of the true SNL can lead to lymph fluid rerouting and, thus, the identification of alternative lymph nodes as being "sentinel," which can lead to a false-negative SLN. The combined use of lymphoscintigraphy and US might allow us to avoid this pitfall, since US will reveal (enlarged) lymph nodes with extensive tumor infiltration.

SLN biopsy is a routine procedure in breast and melanoma studies, but this seems unattractive for squamous cell carcinoma of the head and neck. An open biopsy, which requires an additional operation, is an invasive technique in which other structures, including lymph nodes, might have to be dissected to reach the SLN; this procedure thereby complicates secondary surgical treatment of the neck in the case of a positive SLN. Furthermore, an open biopsy is, in general, considered an indication for postoperative radiation therapy, which could have been avoided in some patients. In contrast to axillary lymph node dissection, selective neck dissection has a relatively low morbidity rate and is widely used as a staging procedure. Although debatable, some authors (17) even consider selective neck dissection as a curative procedure in cases of limited metastatic disease. Therefore, the role of an SLN procedure in the head and neck might, in our opinion, be more attractive if combined with a minimally invasive technique such as US-guided fine-needle aspiration and cytologic examination.

In conclusion, these preliminary data show that US-guided fine-needle aspiration of SLNs is feasible. Whether this approach has the potential to increase the sensitivity of US-guided fine-needle aspiration with cytologic examination for staging in patients with a clinically negative neck (N0) must be determined in a larger series of patients.


   FOOTNOTES
 
Abbreviation: SLN = sentinel lymph node

Author contributions: Guarantors of integrity of entire study, M.W.M.v.d.B., G.B.S.; study concepts, M.W.M.v.d.B., R.P., R.H.B., J.A.C.; study design, M.W.M.v.d.B., R.P., R.H.B., J.A.C., G.B.S.; definition of intellectual content, M.W.M.v.d.B., J.A.C., G.B.S.; literature research, D.R.C., E.J.C.N., M.W.M.v.d.B.; clinical studies, D.R.C., E.J.C.N., R.P., J.A.C.; data acquisition, D.R.C., E.J.C.N.; data analysis, D.R.C., E.J.C.N., R.P.; manuscript preparation, D.R.C., E.J.C.N.; manuscript editing, M.W.M.v.d.B., R.P., R.H.B., J.A.C.; manuscript review, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 

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