Lymphoscintigraphy of Head-and-Neck Cancer M.D. Takashi Terauchi, M.D. Satoshi Ebihara, M.D. Takashi Yoshizumi, M.D. Kazuhiko Mashima, M.D. Masahisa Saikawa, M.D.

Shoji Terui,

Takashi Nakatsuka, M.D. Hiroshi Nishino, M.D.

Yojiro Ota,

M.D.

Kohichi Hirano, M.D. and Ryuichi Hayashi, M.D.

TOKYO, JAPAN

Abstract To achieve the visualization of regional lymph nodes by lymphoscintigraphy, 21 patients with head-and-neck cancer were studied with the aid of 99m Tc-labeled rhenium sulfur colloid Tc 99m Re). Four injection sites were selected; the injec( tions were given into the subcutaneous tissue of the parietal area of 11 patients, into the submucosa of the retromolar area of 6 patients, into the subcutaneous tissue of the postauricular area of 2 patients, and into the thyroid glands of 2 patients. Lymphoscintigraphy was done three hours after the injection. The cervical regions were visible in 85.7% of the patients on the affected side and in 90.5% on the healthy side. The visualization comprised the following regions: submental, submandibular, deep cervical, accessory, and supraclavicular regions. In total, 102 nodes were visualized on the affected side (average 4.8 per patient) and 110 nodes in the healthy side (average 5.5). Histologically, 15 of 21 patients had lymph nodes metastases and 6 did not. Of these 21 patients, 66.7% (14/21) had confirmed lymph node metastases in the visualized regions. This technique appears to be a relatively easy and efficient method of imaging the regional lymph nodes in head-and-neck cancer both before treatment and after neck surgery.

From the Division of Nuclear Medicine and Head and Neck

Surgery Division,

National Cancer Center Hospital,

Japan

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Tokyo,

926

Introduction

spite of the capability of visualizing the cervical lymphatic system in man as reported in the 1960s by Wallace et al,’ Jackson et al,2 and Fisch and del Buono,3 cervical lymphography still presents certain technical problems. With lymphoscintigraphy, we are now able to perform a simple and easy examination of the regional lymph nodes . 4,5 In

Materials and Methods From October, 1990, to March, 1991, we treated 21 head-and-neck cancer cases: 5 patients with tongue cancer, 4 with laryngeal cancer, 4 with thyroid cancer, and 3 with cancer of the oral floor; the others were single cases of parotid cancer, carcinoma of the gingiva, tonsillar cancer, carcinoma of the hypopharynx, and a primary unknown cervical lymph nodes involvement. Five patients had been diagnosed as primary cases but not subjected to treatment, 4 had received radiation to the neck, 5 had received systemic chemotherapy, and 7 were recurrent cases who had had the primary tumors excised (with or without radical neck dissection). The surgical steps undertaken for these 21 patients were as follows: radical neck dissection (RND): 18 patients; axillary node dissection: 1 patient; upper neck dissection: 1; and thyroid lobectomy with a paratracheal and pretracheal nodes dissection: 1.

Injection Methods and Radionuclide To obtain our lymphoscintigrams, we used ~&dquo;’Tc rhenium colloid (99&dquo;Tc Re).6 Four injection sites were selected owing to the nature of the disease coupled with the intention to expose only the necessary minimum of the infected area. Eleven of the 21 patients were given the injection into the subcutaneous tissue of the parietal area (parietal injection); 6, into the submucosa of retromolar area (retromolar injection); 2, into the subcutaneous tissue of the postauricular area (postauricular injection); and 2, into the thyroid glands (thyroid injection). On the day before the projected surgery, a total of 185MBq of 99&dquo;Tc Re in 1 mL was injected into both the affected and its symmetrical healthy side. The four types of injection are executed in the following ways. l. Parietal injection. The patient is put in a supine position and the injection point of the parietal area is fixed on the intersection point of the frontal line of the external auditory canal and sagittal line to the eyes. While one exerts pressure on the parietal skin with the free hand, a 21-gauge, 1.25-inch needle is pushed vertically into the skin, first to the affected side. When the needle reaches the surface of the parietal bone, 0.5 mL of 99&dquo;Tc Re is injected. The same procedure is followed for the healthy side. 2. Retromolar injection. The patient is in a sitting position; A 21-gauge, 1.25-inch needle is pushed into the submucosa of the retromolar area in the direction of the inner side of the mandibular. Then 0.5 mL of 99Tc Re is injected. 3. Postaurical injection. Subcutaneous injection is performed just above the mastoid tip behind the auricular, first to the affected side. The same procedure follows on the healthy side. 4. Thyroid injection. The injection method of 99&dquo;Tc Re is performed according to the method of thyroidlymphography that has been introduced and described by Matoba.’ The needle transverses the stemohyoid muscles to reach the thyroid gland; then 0.5 mL of 99Tc Re is injected.

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927

FIG. lA. An anterior view of the life-size lymphoscintigram obtained from a 65-year-old man who had undergone preoperative radiation therapy (30 Gy for a total of 20 days) for laryngeal cancer with right cervical lymph nodes involvement. The ~&dquo;&dquo;Tc Re was injected into subcutaneous tissue of the parietal area. An even uptake of hot nodes was demonstrated in both sides of cervical regions. The sternal notch is marked on the lymphoscintigram (X). B. The life-size lymphoscintigram superimposed upon the patient’s chest roentgenogram. The roentgen image of an object is larger than the object itself, because of the divergence of the x-rays. There appears, with our method of procedure, only a negligible difference between the life-size lymphoscintigram and the chest roentgen image, thus enhancing an almost exact location. C. A superimposed image (SI). Six hot nodes were noticed on the right cervical (affected side), and 7 nodes on the left (healthy side). Of the 6 nodes on the affected size, we diagnosed the upper 2 nodes to be on the cranial jugular, the middle 2 on the accessory, and the lower 2 on the supraclavicular region accessory. Of the 7 nodes on the healthy side, we diagnosed the upper 1 node to be on the cranial jugular, the middle 3 on the accessory, and the lower 3 on the supraclavicular region. Histologically, lymph node metastases were confirmed in the cranial, medial, and caudal jugular regions.

Lymphoscintigraphy The lymphoscintigraphic images are taken three hours after the injection; an anterior-view lymphoscintigram is obtained on the 11 x 14 inch film with a large-field gamma camera. The collimator is of the low-energy, parallel-hole type and results in at least 1,300,000 counts per image. The injection sites are covered with leaden plates because of high radioactivity. The sternal notch is marked on the film automatically; in this way we are able to obtain a realistic life-size lymphoscintigram (Fig. lA). This life-size lymphoscintigram is then superimposed upon the previously taken posteroantero chest roentgenogram of the patient in the upright position (Fig. 1B)-the clavicles and the contours of the neck are marked with inerasable ink onto the lymphoscintigram (the so-called superimposed image [SI] [Fig. 1C]). The regions of the visualized nodes (hot nodes) are easily assessed according to the WHO classification.9 Afterwards, we count the relevant hot nodes. Scintigram of the Specimen After the surgery, the lymph nodes of the specimens are dissected and divided into the above-mentioned anatomic groups, which are then mapped on the appropriate paper (Fig. 2A, B). All the specimens of lymph nodes of the 21 patients were examined once more scintigraphically to confirm them as actual hot spots. The dissected nodes were then studied histologically. Results The cervical regions were visible in 85.7% (18/21) on the affected side and in 90.5% (19/21) on the healthy side. In these 21 patients, the lymph nodes of 18 could be visualized on

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928 TABLE I

Results

of the Parietal Injection (11Patients)

TABLE II

Results

of Retromolar Injection (6 Patients)

both the affected and the healthy sides; however, the lymph nodes of 2 patients could not be visualized at all; their injection sites were respectively the postauricular and the thyroid area. A patient who had received the retromolar injection had his nodes visualized only on the healthy side; the fact that his affected lymph nodes could not be visualized is most probably due to the positioning of the penetrating needle. No metastatic lesion in cervical nodes was confirmed histologically in those nodes not visualized. Histologically, 15 of 21 patients had lymph nodes metastases and 6 had not. Seven of the 21 patients offered a symmetrical visualization (the healthy and the affected side) of cervical lymph nodes; however, the other 14 showed no symmetrical visualization. In spite of their symmetrical visualization, the 7 patients had the lymph nodes metastases established only

histologically. Uptakes of 99mTc Re in the nodes were even for 11 patients and not even for the other 10 patients. However, no correlation was found between the symmetrical visualization and the even uptake. Moreover, no correlation was seen between the uptake and the existence of lymph nodes metastases. Table I shows results of the parietal injection. Their corresponding lymphostintigrams showed hot nodes spreading to the submental, submandibular, deep cervical (cranial, medial, and caudal) accessory, and supraclavicular regions (Fig. 1 A) . Compared with the lymphoscin-

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929

FIG. 2A. A

superimposed image with 99rn.¡’c

Re at 3

hours after the retromolar injection obtained from a 68year-old man with left cervical node recurrence of the cancer of the oral floor who had undergone resection of the

primary tumor and right upper neck dissection a year before. Asymmetrical visualization was demonstrated in the cervical node because of the surgery as mentioned above. Approximately 12 nodes were observed in the left cervical (affected side). B. Left radical neck dissection was performed and 48 nodes were dissected from the specimen and mapped on the paper (right). Scintigram of the specimen (left) demonstrated 24 hot nodes.

before the surgery, the scintigrams of the specimens after the surgery showed an increased visibility of both the supraclavicular and the accessory regions. An average 3.8 regions per patient (within a range of 2 to 6) were visualized on the affected side, and an average 2.6 regions per patient (in a range of 1 to 5), on the healthy side. An average 6.2 nodes were visualized on the affected side, and 6.4 on the healthy side. Table II shows results of the retromolar injection. In 5 of 6 patients, visualization of the cervical regions on both the affected and the healthy sides was achieved (Fig. 2A). Only in 1

tigrams

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930 TABLE ill

Results

of Postauricular

Injection (2 Patients)

TABLE IV Results

of Thyroid Injection (2 Patients)

patient was the visualization of the nodes on the healthy side alone possible. Thus there was visibility in 83 % of the patients on the affected side and in 100 % on the healthy side. Extraordinarily, 1 patient’s left axillary nodes were definitely visualized in the preoperative lymphoscintigram. Table III shows results of the postauricular injection. Of the 2 patients, only in 1 was visualization of the anterior cervical nodes such as the cranial, medial, and caudal jugular regions on both the affected and the healthy sides possible. The other patient’s node could not be visualized on the scintigram. After the surgery, this patient’s specimen-scintigram showed the hot nodes in the medial jugular, caudal jugular, and the accessory regions. Table IV shows results of the thyroid injection. Of the 2 patients, the nodes of only 1 were visualized in the cranial jugular region of the affected side and in the cranial and medial jugular regions of the healthy side. The other patient’s nodes could not be visualized on the scintigram, owing to the high radioactivity of the injected sides of the thyroid. Table V summarizes the number of the visualized nodes on the scintigram, the number of the dissected nodes in the pertinent specimen, and the number of the specimens with visualized nodes. In total, 102 nodes were visualized on the affected sides (average 4.9 nodes per patient in a range from 1 to 12), as against 110 nodes on the healthy sides (average 5.2 nodes per patient in a range from 1 to 14). In total, 677 nodes were removed operationally from the head-and-neck region, and as many as 189 (27.9 % ) nodes could be perceived on the scintigrams of the postsurgical specimens. In comparison, 15.1 % (102/677) nodes had been visualized on the scintigrams presurgicaHy. Hot nodes of the dissected specimens were also noticed spreading to the prelaryngeal, paratracheal, and parotid nodes-notoriously inaccessible regions.

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931 TABLE V

Correlation

of the Numbers of Lymph Nodes Visualized on

the SI and the Dissected Nodes

TABLE VI

Correlation

of Visibility and Existence of lymph Nodes Metastases

Histologically, metastases were found in 167 of 677 nodes (24.7%). The correlation between the presurgically visualized regions on the scintigrams and the existence of metastases is summarized in Table VI. Of these 21 patients, 66.7 % (14/21) were confirmed as having lymph node metastases in the visualized regions, and 14.3% (3/21) showed no metastases in their visualized regions. On the other hand, only 1 patient (4.8 % ) was confirmed as having lymph node metastases in the nonvisualized regions. Discussion The 99Tc-labeled rhenium sulfur colloid is a new radiopharmaceutical for lymphatic scintigraphy.6 The size of 9&dquo;’Tc Re is smaller than colloidal gold and is uniform 20-40 A. It can be readily prepared and rapidly migrates into the lymph nodes. For the visualization of the cervical lymph nodes by lymphography, cervical lymphoangiography by postaurical cannulation, thyroidlymphography, and tongue lymphoangiography have been used as reported.I-3,7,8 According to Jackson et al, their retroauricular lymphograms allowed visualization of the deep cervical and supraclavicular lymphatic system.~ Moreover, now, our lymphoscintigram of the postauricular injection enables us to visualize the same regions as the postauricular lymphogram. Clinically, however, a lymphoscintigram has the disadvantage of the high radioactivity of the injection sites, which covers the regions we want to see. On the other hand, both the parietal and the retromolar injection enable us to see the

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932 cervical nodes without any disturbance of the activity of the injection sites. In the case of a primary tumor localized in the oral cavity, we consider the retromolar injection to be most appropriate for the injection site, provided it can be performed. Scintigraphically, it still remains difficult to determine which of the visualized nodes or visualized regions contains metastases. Even if the node is completely replaced by cancer cells, it will not appear so. Our own mediastinal lymphoscintigraphy study has shown the incidence of the visualized nodes with esophageal cancer to be 34. 6 % 4; we were able to establish the lymph node metastases only histologically. Now in our present study, 66.7 % ( 14/21 ) of patients have been confirmed as having lymph node metastases in the visualized regions and only 4. 8 % (1/21) as having lymph node metastases in the nonvisualized regions (Table VI). Conclusion For the exact diagnosis of the location of the visualized nodes, our injection technique in conjunction with the superimposed lymphoscintigram provides a rather efficient and easily manageable method for imaging the regional lymph nodes of head-and-neck cancer patients. As for the identification of lymph node metastases with hot nodes on the lymphoscintigram, it is our hypothesis that a radionuclide labeled with a monoclonal antibody might be of special clinical value in the future. 10-12

Acknowledgment This research was supported by CIS Diagnostic Inc., Tokyo, Japan, and was submitted at the 38th Annual Meeting of The American College of Angiology, Maui, Hawaii, 1991.

, M. D. Shoji Terui Division of Nuclear Medicine National Cancer Center Hospital 5-1-1 Tsukiji, Chuo-ku

Tokyo 104, Japan

References 1. Wallace S, Jackson L, Schaffer B, et al: Lymphoangiograms: Their diagnostic and therapeutic potential. Radiology 76:179-199, 1961. 2. Jackson L, Wallace S, Farb S, et al: Cervical lymphography. Laryngoscope 73:926-941, 1963. 3. Fisch UP, del Buono MS: Zur Technik der cervicalen Lymphographie. Schweiz Med Wochenschr 93 :994998, 1963. 4. Terui S, Kato H, Hirashima T, et al: An evaluation of the mediastinal lymphoscintigram for carcinoma of the esophagus studied with Tc-99m rhenium sulfur colloid. Eur J Nucl Med 7:99-101, 1982. 5. Terui S, Yamamoto H: New simplified lymphoscintigraphic technique in patients with breast cancer. J Nucl Med 30:1198-1204, 1989. 6. Pecking A, Le Mercier N, Gobin R, et al: Resultats preliminaires de l’essai d’un nuoveau compose pour lympographies isotopiques: Le sufure de rhenium colloidal marque par du technetium-99m. J Fr Biophys Med Nucl 2:117-120, 1978.

7. Matoba N, Kikushi T: Thyroidlymphography, a new technique for visualization of the thyroid and cervical lymph nodes. Radiology 92:339-342, 1969. 8. Larson DL, Lewis SR, Rapperport AS, et al: Lymphatics of the mouth and neck. Am J Surg 110 :625630, 1965. 9. Seaman WB, Powers WE: Studies in the distribution of radioactive colloidal gold in regional lymph nodes containing cancer. Cancer 8:1044-1046, 1955. 10. Weinstein JN, Steller MA, Covell DG, et al: Monoclonal antitumor antibodies in the lymphatics. Cancer Treat Rep. 68:257-264, 1984. 11. Nelp WB, Eary JF, Jones RF, et al: Preliminary studies of monoclonal antibody lymphoscintigraphy in malignant melanoma. J Nucl Med 28:34-41, 1987. 12. Keena AM, Weinstein JN, Mulshine JL, et al: Immunoscintigraphy in patients with lymphoma after subcutaneous injection of indium 111-labeled T101 monoclonal antibody. J Nucl Med 28:42-46, 1987.

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Lymphoscintigraphy of head-and-neck cancer.

To achieve the visualization of regional lymph nodes by lymphoscintigraphy, 21 patients with head-and-neck cancer were studied with the aid of 99mTc-l...
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