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Indirect cervical lymphoscintigraphy in healthy subjects via submucosal cheek injections
NW/. Med. Biol. Vol. 13, No. 6, pp. 633-637, 1986 Int. J. Radiar. Appl. Insrrum. Parr B
Printed
0883-2897/86 $3.00 + 0.00 Copyright c
1986
Pergamon Journals Ltd
in Great Britain. All rights reserved
Indirect Cervical Lymphoscintigraphy in Healthy Subjects via Submucosal Cheek Injections S. TZILA ZWAS’ and YOCHANAN
RAMON’
Departments of ‘Nuclear Medicine and 20ral Surgery, The Chaim Sheba Medical Center, Tel-Hashomer, Sackler School of Medicine, and 2School of Dental Medicine, Tel-Aviv University, Israel (Received
15 April 1986)
A new method of cervical lymphoscintigraphy is presented. It was performed on 16 healthy individuals via bilateral submucosal cheek injections with vc-rhenium-sulfide-colloid. The ipsilateral uptake by the lymphatics on each side of the neck was consistently demonstrated in 15 subjects and allowed a comparative evaluation of the cervical lymphatic chains, including the submental, submandibular, jugulo-digastric and jugulo-omohyoid. The transverse cervical chain was demonstrated in 10 of 16 subjects. The method is simple, reliable and capable of clearly visualizing the lymphatic drainage of the oral cavity.
Introduction The cervical lymphatic channels and nodes drain the oral cavity and the upper aerodigestive tract, the so-called head and neck region. It plays a major defence role in infectious conditions, in benign lesions and in cancerous metastases of the head and neck. The state of the cervical lymphatics has a major significance in the treatment planning and in the prognosis of head and neck malignancies. Direct lymphography and lymphoscintigraphy of the tongue and floor of the mouth have been used in studies aiming at the visualization of the cervical lymphatics. The results were inconsistent and of little clinical value.““) The tongue and floor of the mouth have an extremely rich lymphatic supply and are in constant movement which promotes lymphatic flow. This results in extensive ipsilateral drainage to the anterior and often to the posterior triangle and even to the contralateral side. Hence, direct or indirect lymphography of the tongue and the floor of the mouth visualizes the overall cervical lymphatic net with considerable superposition, rendering image interpretation of individual glands very difficult if not impossible.(‘) In contrast to the tongue and floor of the mouth, lymphatic drainage of the cheek is always ipsilateral to the major lymph nodes of the anterior triangle of Address for correspondence: S. Tzila Zwas, M.D., Dept. of Nuclear Medicine, The Chaim Sheba Medical Center, Tel-Hashomer 5262 1, Israel.
the neck, and hence it may be assumed that lymphoscintigraphy via the cheeks should clearly visualize the main lymphatic drainage of the oral cavity.“) The purpose of the present study was to establish a non-invasive, safe, simple and reliable lymphoscintigraphic method to visualize normal lymphatic drainage of the oral cavity and to study the normal physiological state of the cervical lymphatic system.
Material and Methods Sixteen healthy volunteers, seven females and nine males, mean age 43 years (range 2@-76), consented to participate in the study. (a) Preparation
and administration
of rhenium -sul$de-
colloid
The 99mTc-rhenium-su1phide-colloid ( 99mTc-Rh SC) was prepared from a “lymphocis” kit-TCK17(CIS Co.). One-half milliliter of dissolved tinpyrophosphate was added to 1 mL rhenium sulphide solution. [ 99mTc]pertechnetate (1.5 mL) containing 20 mCi/mL was added to the mixture, which was then immersed in boiling water for 30min. A brown colloidal suspension was obtained and, after cooling, 0.3 mL aliquots containing 2-3 mCi WmT~were prepared in 1 mL tuberculine syringes. Three 0.1 mL submucosal injections of the cheek, about 0.5-l cm apart, at the level of the occlusal plane, were given with a 25 gauge needle (Fig. 1). Immediately following the injections, the cheeks were massaged and the 633
S. TZILA ZWAS and YOCHANANRAMON
634
Results
INJECTION
SITES
Fig. 1. The site of the submucosal cheek injections at the level of the occlusal plane.
subject was instructed to rinse his mouth thoroughly in order to avoid swallowing any escaped material. The subject was instructed to drink 2-4 glasses of water, eat a salted meat sandwich and sweets and to chew gum in order to accelerate the lymphatic flow and drainage. (6)No discomfort or untoward effects were noted in any of the subjects.
(b) Lymphoscintigraphic
method
Scintigrams of the neck were obtained at 2 and 24 h after the injections. The subjects were placed in a supine position and images were taken with an LFOV gamma camera using a high-resolution collimator. The neck was visualized anteriorly and from both lateral positions. Two images were taken from each position, one with and one without a lead shield covering the injection sites. About 200,000 counts were accumulated from each view, in each position. Two scintigraphic parameters were evaluated by visual inspection: the radiocolloid concentration within the visualized nodes and their symmetrical distribution in the neck. Two physicians evaluated the radiocolloid concentration within the cervical nodes by visual comparison with the maximal concentration in the proximal submandibular nodes as follows: positive-when the lymph-node concentration was comparable to or somewhat lower than that in the submandibular nodes; negative-when the glands, expected to be in the normal anatomical sites, were not visualized.
When summarizing the personal data and the lymphoscintigraphic results, it was noted that neither sex nor age had any significant bearing. In 15 out of the 16 subjects, the submental, submandibular, jugulo-digastric and jugulo-omohyoid nodes (Fig. 2). were clearly visualized (positive) and a symmetrical cervical visualization was demonstrated in 13 out of 16 subjects (Figs 3 and 4). The transverse (lower) cervical chain was visualized in 10 out of 16 subjects. The lymphoscintigrams obtained 2 h post injection (see Fig. 3) showed discrete lymph node aggregates and chains in sequential bilateral patterns of distribution in the submandibular region and along the upper region of the jugular vein with minimal variability in size. An overall positive radiocolloid concentration and clear symmetrical glands were visualized in nearly all the lymph node groups (chains). In the lower cervical glands positive visualization was less consistent. Taking into consideration that every subject presented five groups of glands on each side of the neck, positive visualization was obtained in 89% of the gland groups (142 out of 160) while 11% of the gland groups, mainly the transverse cervical glands, were not visualized (Table 1). There was usually a slight and gradual decrease in radiocolloid node concentration in direct relation to the distance from the sites of injection (see Figs 3 and 4). The lymphatic channels were often seen clearly on 2-h scans, while some enhancement in lymph node visualization was noted on 24-h scans.
Discussion Postmortem anatomical visualization studies of the cervical lymphatics have been performed since the 18th century, (*)but our current knowledge is based on Rouvier’s study in 1932.(9) He delineated the lymphatic channels and nodes in freshly prepared human cadaveric specimens by injecting oil colors dissolved in turpentine and ether into lymphatic vessels. Recent studies confirmed his findings.“&“) The anatomic studies revealed that lymphatic drainage of the oral cavity is limited mainly to lymph nodes in the anterior triangle of the neck and the upper part of the deep jugular lymphatic chain. The submental, submandibular, jugulo-digastric and jugulo-omohyoid nodes are the four main lymphatic
Table 1. Frequency of bilateral lymph node chain visualization in 16 normal subjects No. of bilateral chains Lymph node chain SUBMANOlBULAR
-TRANSVERSE
(lower)
CERVICAL
Fig. 2. Schematic presentation of the major cervical lymphatic chains and nodes in right lateral view.
Submental Submandibular J&o-digastric Jugulo-omohyoid Transverse cervical Total
Possible 32 32 32 32 32 lao(loo%)
Visualized 32 32 30 31 17 142 (89%)
ANT
ANT
Inj.
site
LLAT
LLAT
4
RLAT
”
RLAT
Fig. 3. %Tc-Rh SC lymphoscintigraphic study of the neck is demonstrated in anterior and bilateral views (2 h post injections) in panel A-injection sites are covered and anatomical marking of the ears, chin and sternal notch is shown; in panel B-injection sites are uncovered (large arrowheads) for image comparisons, collecting the same counts per view. In the lateral views, ipsilateral chains (large arrows) and contralateral chains (small arrows) are demonstrated separately.
635
I
MARK
MARK
RLAT
LLAT
Fig. 4. *Tc-Rh SC lymphoscintigraphy of the neck in bilateral views (24 h post injections). The injection sites are covered and the sternal notch (V) is marked. There is symmetric visualization of the ipsilateral proximal and distal glands (large arrowheads) with faint contralateral lymphatics visualization in each view (small arrowheads).
636
Indirect
cervical
draining nodes of the oral cavity, while the transverse cervical chain drains the posterior triangle (deep accessory nodes) and indirectly the lower deep cervical nodes as we11.u4’These findings were confirmed by clinical oncological experience(i5~i6) and studies of large series of oral carcinoma have shown that the first four lymphatic nodes were involved in 85-88% of all secondary cervical metastatic deposits.(‘7-‘9) The introduction of radiological methods using direct lymphography in humans paved the way to extensive studies of the lymphatic system, including the head and neck region.‘“) These studies were carried out by the injection of radio-opaque materials into lymphatic vessels of the tongue and floor of the mouth. The findings of these studies, demonstrated an extensive complex of ipsilateral and contralateral drainage pathways of the floor of the mouth and tongue.“,“.22
Radiocolloid lymphoscintigraphy introduced in the early 60’s has proven to be a simple, safe and reliable method and has been used extensively ever sincc,(23~24) and is applicable to all sites of the oral cavity. Indirect lymphoscintigraphy demonstrates the active transfer of the radioactive colloid material by macrophages in the lymph channels and the uptake by the nodal reticuloendothelial cells in addition to passive transfer by the lymph flo~.(‘“,~~) In contrast, direct lymphography, demonstrates the anatomical distribution of passively introduced contrast materia1.‘20*24’ In conclusion, indirect lymphoscintigraphy visualizes the physiological parameters of the lymphatic system: lymphatic flow, reticuloendothelial hyperplasia, and immune enhancement. The lymphoscintigrams achieved by submucosal injection of the cheeks visualized drainage of the oral cavity. It showed the position of the lymphatic chains, allowed a comparative study of the two sides of the neck, and provided information regarding the lymph flow and the uptake by the glandular reticuloendothelial system. The presented method, which consistently visualized the groups of lymph nodes draining the oral cavity, confirmed unequivocally the anatomical studies(‘S’3) of oral lymphatic drainage. It also clarified the clinical observation that 85-88% of all secondary metastatic deposits in the neck originating from oral mucosal carcinoma involve these four groups of glands.(‘5-‘9) The presented method of lym-
lymphoscintigraphy
631
phoscintigraphy should find wide clinical application in the evaluation and management of cervical lymphoadenopathies especially in oral cancer patients. Acknowledgemenfs-The authors are thankful to Lionel M. Lieberman, M.D., Ph.D. for reviewing the manuscript and gratefully acknowledge the technical assistance of the staff of the Department of Nuclear Medicine.
References 1. Winkel K. Z. and Herman H. J. Lymphology 10, 107 (1977). R. W., McConnell B. G. and Kim E. E. 2. McConnell Semin. Nucl. Med. 13, 70 (1983). H. J. Fortschr. Rontgenstr. 106, 524 (1967). 3. Femholtz P. 4. Tommesen P., Buhl J., Jansen K. and Fuch-Janscn Fortschr. Roenrgenstr. 134, 80 (1981). M. Laryng. Rhinol. 55, 575 5. Stutte H. J. and Amaudow (1976). F. Lymphology 12, 6. Thommesen P. and Taagehoj-Jensen 108 (1979). 7. Asarch R. G. J. Dermatol. Stag. Oncol. 8, 869 (1982). 8. Yoffev J. M. and Courtice F. C. Lvmphatics, Lvmph and _ . the Lymphoid Complex (Academic Press, ‘London, 1980). 9. Rouvier H. Anatomic des Lymphatiques de I8 Hommes (Masson & Cie, Paris, 1932). IO. Larson D. L. Am. J. Stag. 110, 625 (1965). 11. Welsh L. W. and Welsh J. J. Ann. Otolarvnnol. , - 15. 116 (1966). 12. Guart F. J., Yoel J. and Wagner A. M. Am. J. Surg. 114, 520 (1967). 91, 13. Ossoff R. H. and Sisson G. A. The Laryngoscope 1847 (1981). 14. Reed G. M. and Sheppard A. B. Basic Structures the Head and Neck (W. B. Saunders, Philadelphia, 1976). 15. Pinborg J. J. Oral Cancer and Precancer (John Wright, Bristol, 1980). 16. Shafer W. G., Hine M. K. and Levy B. M. A Texlbook of Oral Pathology (W. B. Saunders, New York, 1983). 17. Lindberg R. Cancer 29, 1446 (1972). 18. Spiro R. H., Alfonso A. E. and Farr H. W. Am. J. Surg. 128, 562 (1974). 19. Yamamoto E., Miyakawa A. and Kohama G. I. Head and Neck Surg. 6, -938 (1984). J. R. Ann. R. CON. Stag. 14, 300 (1954). 20. Kinmouth F. L., Sako K. and Badillo J. Am. J. Stag. 21. Marchetta 108, 505 (1974). 22. Ossoff R. H.. Bvtell D. E. and Sisson G. A. Orolarvnnol. I Y Head Neck %g. 88, 652 (1980). L. D. and Joseph C. D. Tumor Imaging 23 Greenfield (Masson, New York, 1982). S. Semin. 24. Croll M. N., Brady L. W. and Dadparvar Nucl. Med. 13, 4 (1983).
of
Printed
0883-2897/86 $3.00 + 0.00 Copyright c
1986
Pergamon Journals Ltd
in Great Britain. All rights reserved
Indirect Cervical Lymphoscintigraphy in Healthy Subjects via Submucosal Cheek Injections S. TZILA ZWAS’ and YOCHANAN
RAMON’
Departments of ‘Nuclear Medicine and 20ral Surgery, The Chaim Sheba Medical Center, Tel-Hashomer, Sackler School of Medicine, and 2School of Dental Medicine, Tel-Aviv University, Israel (Received
15 April 1986)
A new method of cervical lymphoscintigraphy is presented. It was performed on 16 healthy individuals via bilateral submucosal cheek injections with vc-rhenium-sulfide-colloid. The ipsilateral uptake by the lymphatics on each side of the neck was consistently demonstrated in 15 subjects and allowed a comparative evaluation of the cervical lymphatic chains, including the submental, submandibular, jugulo-digastric and jugulo-omohyoid. The transverse cervical chain was demonstrated in 10 of 16 subjects. The method is simple, reliable and capable of clearly visualizing the lymphatic drainage of the oral cavity.
Introduction The cervical lymphatic channels and nodes drain the oral cavity and the upper aerodigestive tract, the so-called head and neck region. It plays a major defence role in infectious conditions, in benign lesions and in cancerous metastases of the head and neck. The state of the cervical lymphatics has a major significance in the treatment planning and in the prognosis of head and neck malignancies. Direct lymphography and lymphoscintigraphy of the tongue and floor of the mouth have been used in studies aiming at the visualization of the cervical lymphatics. The results were inconsistent and of little clinical value.““) The tongue and floor of the mouth have an extremely rich lymphatic supply and are in constant movement which promotes lymphatic flow. This results in extensive ipsilateral drainage to the anterior and often to the posterior triangle and even to the contralateral side. Hence, direct or indirect lymphography of the tongue and the floor of the mouth visualizes the overall cervical lymphatic net with considerable superposition, rendering image interpretation of individual glands very difficult if not impossible.(‘) In contrast to the tongue and floor of the mouth, lymphatic drainage of the cheek is always ipsilateral to the major lymph nodes of the anterior triangle of Address for correspondence: S. Tzila Zwas, M.D., Dept. of Nuclear Medicine, The Chaim Sheba Medical Center, Tel-Hashomer 5262 1, Israel.
the neck, and hence it may be assumed that lymphoscintigraphy via the cheeks should clearly visualize the main lymphatic drainage of the oral cavity.“) The purpose of the present study was to establish a non-invasive, safe, simple and reliable lymphoscintigraphic method to visualize normal lymphatic drainage of the oral cavity and to study the normal physiological state of the cervical lymphatic system.
Material and Methods Sixteen healthy volunteers, seven females and nine males, mean age 43 years (range 2@-76), consented to participate in the study. (a) Preparation
and administration
of rhenium -sul$de-
colloid
The 99mTc-rhenium-su1phide-colloid ( 99mTc-Rh SC) was prepared from a “lymphocis” kit-TCK17(CIS Co.). One-half milliliter of dissolved tinpyrophosphate was added to 1 mL rhenium sulphide solution. [ 99mTc]pertechnetate (1.5 mL) containing 20 mCi/mL was added to the mixture, which was then immersed in boiling water for 30min. A brown colloidal suspension was obtained and, after cooling, 0.3 mL aliquots containing 2-3 mCi WmT~were prepared in 1 mL tuberculine syringes. Three 0.1 mL submucosal injections of the cheek, about 0.5-l cm apart, at the level of the occlusal plane, were given with a 25 gauge needle (Fig. 1). Immediately following the injections, the cheeks were massaged and the 633
S. TZILA ZWAS and YOCHANANRAMON
634
Results
INJECTION
SITES
Fig. 1. The site of the submucosal cheek injections at the level of the occlusal plane.
subject was instructed to rinse his mouth thoroughly in order to avoid swallowing any escaped material. The subject was instructed to drink 2-4 glasses of water, eat a salted meat sandwich and sweets and to chew gum in order to accelerate the lymphatic flow and drainage. (6)No discomfort or untoward effects were noted in any of the subjects.
(b) Lymphoscintigraphic
method
Scintigrams of the neck were obtained at 2 and 24 h after the injections. The subjects were placed in a supine position and images were taken with an LFOV gamma camera using a high-resolution collimator. The neck was visualized anteriorly and from both lateral positions. Two images were taken from each position, one with and one without a lead shield covering the injection sites. About 200,000 counts were accumulated from each view, in each position. Two scintigraphic parameters were evaluated by visual inspection: the radiocolloid concentration within the visualized nodes and their symmetrical distribution in the neck. Two physicians evaluated the radiocolloid concentration within the cervical nodes by visual comparison with the maximal concentration in the proximal submandibular nodes as follows: positive-when the lymph-node concentration was comparable to or somewhat lower than that in the submandibular nodes; negative-when the glands, expected to be in the normal anatomical sites, were not visualized.
When summarizing the personal data and the lymphoscintigraphic results, it was noted that neither sex nor age had any significant bearing. In 15 out of the 16 subjects, the submental, submandibular, jugulo-digastric and jugulo-omohyoid nodes (Fig. 2). were clearly visualized (positive) and a symmetrical cervical visualization was demonstrated in 13 out of 16 subjects (Figs 3 and 4). The transverse (lower) cervical chain was visualized in 10 out of 16 subjects. The lymphoscintigrams obtained 2 h post injection (see Fig. 3) showed discrete lymph node aggregates and chains in sequential bilateral patterns of distribution in the submandibular region and along the upper region of the jugular vein with minimal variability in size. An overall positive radiocolloid concentration and clear symmetrical glands were visualized in nearly all the lymph node groups (chains). In the lower cervical glands positive visualization was less consistent. Taking into consideration that every subject presented five groups of glands on each side of the neck, positive visualization was obtained in 89% of the gland groups (142 out of 160) while 11% of the gland groups, mainly the transverse cervical glands, were not visualized (Table 1). There was usually a slight and gradual decrease in radiocolloid node concentration in direct relation to the distance from the sites of injection (see Figs 3 and 4). The lymphatic channels were often seen clearly on 2-h scans, while some enhancement in lymph node visualization was noted on 24-h scans.
Discussion Postmortem anatomical visualization studies of the cervical lymphatics have been performed since the 18th century, (*)but our current knowledge is based on Rouvier’s study in 1932.(9) He delineated the lymphatic channels and nodes in freshly prepared human cadaveric specimens by injecting oil colors dissolved in turpentine and ether into lymphatic vessels. Recent studies confirmed his findings.“&“) The anatomic studies revealed that lymphatic drainage of the oral cavity is limited mainly to lymph nodes in the anterior triangle of the neck and the upper part of the deep jugular lymphatic chain. The submental, submandibular, jugulo-digastric and jugulo-omohyoid nodes are the four main lymphatic
Table 1. Frequency of bilateral lymph node chain visualization in 16 normal subjects No. of bilateral chains Lymph node chain SUBMANOlBULAR
-TRANSVERSE
(lower)
CERVICAL
Fig. 2. Schematic presentation of the major cervical lymphatic chains and nodes in right lateral view.
Submental Submandibular J&o-digastric Jugulo-omohyoid Transverse cervical Total
Possible 32 32 32 32 32 lao(loo%)
Visualized 32 32 30 31 17 142 (89%)
ANT
ANT
Inj.
site
LLAT
LLAT
4
RLAT
”
RLAT
Fig. 3. %Tc-Rh SC lymphoscintigraphic study of the neck is demonstrated in anterior and bilateral views (2 h post injections) in panel A-injection sites are covered and anatomical marking of the ears, chin and sternal notch is shown; in panel B-injection sites are uncovered (large arrowheads) for image comparisons, collecting the same counts per view. In the lateral views, ipsilateral chains (large arrows) and contralateral chains (small arrows) are demonstrated separately.
635
I
MARK
MARK
RLAT
LLAT
Fig. 4. *Tc-Rh SC lymphoscintigraphy of the neck in bilateral views (24 h post injections). The injection sites are covered and the sternal notch (V) is marked. There is symmetric visualization of the ipsilateral proximal and distal glands (large arrowheads) with faint contralateral lymphatics visualization in each view (small arrowheads).
636
Indirect
cervical
draining nodes of the oral cavity, while the transverse cervical chain drains the posterior triangle (deep accessory nodes) and indirectly the lower deep cervical nodes as we11.u4’These findings were confirmed by clinical oncological experience(i5~i6) and studies of large series of oral carcinoma have shown that the first four lymphatic nodes were involved in 85-88% of all secondary cervical metastatic deposits.(‘7-‘9) The introduction of radiological methods using direct lymphography in humans paved the way to extensive studies of the lymphatic system, including the head and neck region.‘“) These studies were carried out by the injection of radio-opaque materials into lymphatic vessels of the tongue and floor of the mouth. The findings of these studies, demonstrated an extensive complex of ipsilateral and contralateral drainage pathways of the floor of the mouth and tongue.“,“.22
Radiocolloid lymphoscintigraphy introduced in the early 60’s has proven to be a simple, safe and reliable method and has been used extensively ever sincc,(23~24) and is applicable to all sites of the oral cavity. Indirect lymphoscintigraphy demonstrates the active transfer of the radioactive colloid material by macrophages in the lymph channels and the uptake by the nodal reticuloendothelial cells in addition to passive transfer by the lymph flo~.(‘“,~~) In contrast, direct lymphography, demonstrates the anatomical distribution of passively introduced contrast materia1.‘20*24’ In conclusion, indirect lymphoscintigraphy visualizes the physiological parameters of the lymphatic system: lymphatic flow, reticuloendothelial hyperplasia, and immune enhancement. The lymphoscintigrams achieved by submucosal injection of the cheeks visualized drainage of the oral cavity. It showed the position of the lymphatic chains, allowed a comparative study of the two sides of the neck, and provided information regarding the lymph flow and the uptake by the glandular reticuloendothelial system. The presented method, which consistently visualized the groups of lymph nodes draining the oral cavity, confirmed unequivocally the anatomical studies(‘S’3) of oral lymphatic drainage. It also clarified the clinical observation that 85-88% of all secondary metastatic deposits in the neck originating from oral mucosal carcinoma involve these four groups of glands.(‘5-‘9) The presented method of lym-
lymphoscintigraphy
631
phoscintigraphy should find wide clinical application in the evaluation and management of cervical lymphoadenopathies especially in oral cancer patients. Acknowledgemenfs-The authors are thankful to Lionel M. Lieberman, M.D., Ph.D. for reviewing the manuscript and gratefully acknowledge the technical assistance of the staff of the Department of Nuclear Medicine.
References 1. Winkel K. Z. and Herman H. J. Lymphology 10, 107 (1977). R. W., McConnell B. G. and Kim E. E. 2. McConnell Semin. Nucl. Med. 13, 70 (1983). H. J. Fortschr. Rontgenstr. 106, 524 (1967). 3. Femholtz P. 4. Tommesen P., Buhl J., Jansen K. and Fuch-Janscn Fortschr. Roenrgenstr. 134, 80 (1981). M. Laryng. Rhinol. 55, 575 5. Stutte H. J. and Amaudow (1976). F. Lymphology 12, 6. Thommesen P. and Taagehoj-Jensen 108 (1979). 7. Asarch R. G. J. Dermatol. Stag. Oncol. 8, 869 (1982). 8. Yoffev J. M. and Courtice F. C. Lvmphatics, Lvmph and _ . the Lymphoid Complex (Academic Press, ‘London, 1980). 9. Rouvier H. Anatomic des Lymphatiques de I8 Hommes (Masson & Cie, Paris, 1932). IO. Larson D. L. Am. J. Stag. 110, 625 (1965). 11. Welsh L. W. and Welsh J. J. Ann. Otolarvnnol. , - 15. 116 (1966). 12. Guart F. J., Yoel J. and Wagner A. M. Am. J. Surg. 114, 520 (1967). 91, 13. Ossoff R. H. and Sisson G. A. The Laryngoscope 1847 (1981). 14. Reed G. M. and Sheppard A. B. Basic Structures the Head and Neck (W. B. Saunders, Philadelphia, 1976). 15. Pinborg J. J. Oral Cancer and Precancer (John Wright, Bristol, 1980). 16. Shafer W. G., Hine M. K. and Levy B. M. A Texlbook of Oral Pathology (W. B. Saunders, New York, 1983). 17. Lindberg R. Cancer 29, 1446 (1972). 18. Spiro R. H., Alfonso A. E. and Farr H. W. Am. J. Surg. 128, 562 (1974). 19. Yamamoto E., Miyakawa A. and Kohama G. I. Head and Neck Surg. 6, -938 (1984). J. R. Ann. R. CON. Stag. 14, 300 (1954). 20. Kinmouth F. L., Sako K. and Badillo J. Am. J. Stag. 21. Marchetta 108, 505 (1974). 22. Ossoff R. H.. Bvtell D. E. and Sisson G. A. Orolarvnnol. I Y Head Neck %g. 88, 652 (1980). L. D. and Joseph C. D. Tumor Imaging 23 Greenfield (Masson, New York, 1982). S. Semin. 24. Croll M. N., Brady L. W. and Dadparvar Nucl. Med. 13, 4 (1983).
of