The First Branchial Cleft Carcinoma Stephen
S.
Park, MD, Collin S. Karmody,
Primary branchiogenic carcinoma was previously a deentity. Initially it was a popular diagnosis for many carcinomas of the neck. Then, in 1950, stringent cricystic teria were defined for establishing the diagnosis of primary branchiogenic carcinoma. Only a limited number of cases have successfully fulfilled these criteria. We describe a pa\s=b\
bated
tient who meets the criteria and who we believe represents the first reported case of a carcinoma arising from the vestigium of the first branchial cleft. We also review the literature on branchial cleft carcinomas and discuss the diagnosis, histopathologic features, and therapeutic options. (Arch Otolaryngol Head Neck Surg. 1992;118:969-971)
than 100 years ago, Von Volkman1 claimed that had arisen from the epithelial lining of Morecarcinoma of the branchial He three a a
apparatus. reported vestigium cases of cystic, squamous cell carcinoma in the neck that had not arisen from any obvious primary lesions and sug¬ gested that they were neoplasms of branchial cleft origin. The diagnosis of primary branchial cleft carcinoma (BCC) quickly gained popularity. About 50 years and 250 cases of
BCC later, Martin et al2 reviewed the literature and concluded that such a diagnosis, however convenient, was premature and inaccurate. In fact, they argued that only three reports, by Oliver,3 provided reasonable evidence for carcinomas arising from branchial arch vestigia. Martin and colleagues argued that lengthy disease-free survival is pivotal in order to rule out the late appearance of a primary focus of tumor of the upper aerodigestive tract. Five-year tumor-free survival is believed to provide "reasonable" evidence that no occult primary tumor exists. Martin and coworkers established four criteria to be fulfilled in order to establish a diagnosis of BCC: (1) the tumor should oc¬ cur where branchial clefts are found, ie, along a line from the tragus, down the anterior border of the sternocleido¬ mastoid muscle, to the clavicle; (2) the histologie appear¬ ance of the lesion should be consistent with tissue known to be present in branchial vestigia; (3) the patient must survive for 5 years with consistent examinations and no evidence of a primary focus; and (4) there should be his¬ tologie proof that the carcinoma arises directly from nor¬ mal cyst epithelium. The fourth criterion is thought to be
Accepted for publication June 2, 1992. From the Department of Otolaryngology, New England Medical Cen-
ter, Tufts University School of Medicine, Boston, Mass. Reprint requests to New England Medical Center, PO Box 850, 750
Washington St, Boston,
MA 02111 (Dr
Karmody).
MD
sine qua non for the diagnosis of BCC. With that in mind, Martin and colleagues concluded that no cases to date were definitive proof of the existence of a carcinoma of bran¬
chiogenic origin.
Since 1950 there have been a limited number of case
re¬
ports in which it was stated that the carcinomas originated from the epithelial lining of branchial cysts, and fewer still
that satisfy Martin and coworkers'2 criteria.4"14 All the pub¬ lished cases describe an epidermoid carcinoma in the re¬ gion of the second branchial apparatus. We describe another patient who satisfies Martin and colleagues' crite¬ ria and who we believe represents the first case of carcinoma arising from the first branchial vestigium. REPORT OF A CASE A 23-year-old woman presented with a 5-month history of in¬ tractable pain in the right preauricular area. The pain was dull, radiated to the face, and was not exacerbated by mastication. The patient denied prior trauma, otorrhea, hearing loss, dysphagia, and hoarseness. She had been treated elsewhere with antibiotics for otitis externa and with intermaxillary wiring for temporo¬ mandibular joint dysfunction. She had a 3-pack-year history of smoking and drank alcohol only occasionally. On examination there was a subtle fullness in the area of the right parotid gland, with moderate tenderness and mild trismus. Her neck, tympanic membrane, oral cavity, and pharynx were normal. The external auditory canal revealed a small pit on the anterior floor of the meatal skin, to which a probe could be passed to 1 cm. No puru¬ lence could be expressed from either the pit or Stensen's duct. All cranial nerves were intact. The diagnosis was an infected first branchial cleft duplication anomaly, and intravenous antibiotic therapy was initiated. After 5 days there was no clinical improve¬ ment. A computed tomographic scan then revealed a smooth, circular lucency in the deeper right parotid gland (Fig 1). Surgi¬ cal excision was recommended, and after consenting to the pro¬ cedure, the patient was taken to the surgical suite, where the right parotid gland was explored via the usual approach. Intraopera¬ tively a lxl-cm firm mass was found immediately deep to the facial nerve, clearly involving the buccal branch. There was a tract extending from the cyst toward the ear canal. The patient under¬ went a total parotidectomy with sacrifice of the buccal division. A postoperative facial paresis eventually resolved, and the patient was relieved of the facial pain. The final pathologic diagnosis was invasive squamous cell carcinoma arising from a first branchial cleft cyst. She received postoperative radiation therapy (65 Gy) to the right parotid bed and now, 7 years later, is doing well and is free of tumor.
PATHOLOGIC FINDINGS the lesion was an encapsulated cyst within pa¬ Grossly rotid tissue. Histologically there was a nonspecific chronic
Downloaded From: http://archotol.jamanetwork.com/ by a University of Pennsylvania User on 05/14/2015
Fig 3.—Photomicrograph showing the benign stratified squamous epi¬ thelium with keratin debris (hematoxyling-eosin, original magnification XI00).
Fig 1.—Axial-image computed tomogram showing lucent lesion deep right parotid gland.
in
the
Fig 4.—Invasive squamous cell carcinoma shown to evolve directly from neighboring benign epithelium (hematoxylin-eosin, original magnifica¬ tion X100).
Fig 2.—Low-power photomicrograph demonstrating the cystic nature of the
parotid lesion (hematoxylin-eosin, original magnification X40).
sialadenitis with acinar atrophy and a cystic structure con¬ taining keratin debris (Fig 2). The cyst was lined with benign, keratinizing stratified squamous epithelium (Fig 3). In some foci, however, this benign epithelium was observed to evolve directly into an infiltrating, well-differentiated squamous cell carcinoma (Fig 4). Local inflammation sur¬ rounded the invading tumor edge. There was soft-tissue ex¬ tension as well as intraneural and perineural infiltration by rumor
(Fig 5).
COMMENT Anomalies of the first branchial cleft are categorized into four variants: (1) aplasia, (2) atresia, (3) stenosis, and (4) du¬ The duplication anomaly is found in two forms, plication.15 and 1 type 2. They both have a well-formed external au¬ type 1 ditory canal, but in addition there is a second tract. Type is a duplication of the membranous canal and
Fig 5.—Neural tissue containing metastaticXsquamous (hematoxylin-eosin, original magnification 100).
Downloaded From: http://archotol.jamanetwork.com/ by a University of Pennsylvania User on 05/14/2015
cell carcinoma
usually is found either anterior or posterior to the pinna, running parallel to the canal until exiting in the medial ca¬ nal or, rarely, in the middle ear space. Type 2 is a dupli¬ cation of the membranous canal and is composed of ecto¬ derm and mesoderm, running from the infra-auricular area superiorly toward the canal. It frequently courses deep within the parotid gland and may interwind between
the branches of the facial nerve. Both types are rare clini¬ cal findings, with only about 50 reported cases.16 The incomplete obliteration of any branchial tract will result in a sinus or cyst. The cyst is lined with an epidermal derivative, usually stratified squamous epi¬ thelium. It is possible for carcinomatous degeneration of the cyst lining to occur. However, it is unreasonable to assume such a diagnosis based merely on the finding of a cystic, cervical carcinoma without a primary focus of tumor. The controversy arises from the facts that (1) the jugular lymphatics and most branchial cysts are found in similar regions; (2) metastic squamous carcinoma is expected to occur with far greater frequency than a primary branchiogenic carcinoma; (3) a cervical metasta¬ sis may be the presentation of an occult lesion that only later presents itself in the upper aerodigestive tract; and (4) histologically it is difficult to distinguish a BCC from the cystic degeneration of a metastatic cervical node. Krogdahl17 made histologie comparisons between 154 branchial cleft cysts and normal lymph nodes. She de¬ scribed several characteristics that they share, but she also noted three features that are exclusive to lymph nodes: peripheral lobulation, internodular trabeculae, and perinodular sinuses. There is clinical relevance in distinguishing BCC from metastatic squamous cell car¬ cinoma in that careless reassurance, therapeutic compla¬ cency, and needless overtreatment are all to be avoided. A patient must survive tumor free for 5 years to fulfill the third criterion of Martin et al.2 Therapeutic decisions are made at the time of diagnosis, however, not after the 5-year requirement is satisfied. Postoperative radia¬ tion therapy is used to extirpate residual microscopic disease. This treatment option extends to the squamous carcinomas of branchiogenic origin. When a patient pre¬ sents with a cystic, squamous cell carcinoma, potentially of branchiogenic origin, oncologie excision followed by
is a sound therapeutic option. Our patient represents another case of branchiogenic carcinoma and we believe is the first one reported to have such a lesion of the first branchial apparatus. She had a type 1 duplication anomaly of the first branchial cleft with carcinomatous degeneration arising directly from normal squamous epithelium, and she fulfilled the criteria estab¬ lished by Martin and colleagues. The nonspecific sialad¬ enitis and perineural invasion presumably accounted for her pain. Postoperative radiotherapy was elected because a radical oncologie excision was not possible without mas¬ sive disfigurement. Our patient remains disease free 7 years after her initial presentation.
radiotherapy
References 1. Von Volkmann R. Das tiefe branchiogege Halskarcinom. Zentralbl Chir.
1882;9:49-63. 2. Martin H, Morfit HM, Erlich H. The case for branchiogenic cancer (malignant brachioma). Ann Surg. 1950;132:867-887. 3. Oliver RL. Malignant epithelial tumors of the neck: carcinoma of branchiogenic origin. Am J Cancer. 1935;23:16. 4. Hill FT, Goodof II. Branchiogenic carcinoma. Ann Otol Rhinol Laryngol. 1952;61:474-482. 5. Stackpole RH, Pearce JM. Branchial cleft carcinoma. Arch Surg. 1961; 82:347-352. 6. Schuring A, Arthur J. Branchiogenic carcinoma does exist. Throat Mon. 1967;46:752-753. 7. Katubig C, Damjanov I. Branchial cleft carcinoma. Arch
Eye Ear Nose
Otolaryngol.
1969;89:92-93. 8. Benisch BM, Som ML. Branchial cleft carcinoma. Arch Otolaryngol. 1973;98:208-209. 9. Compagno J, Hyams VJ, Safavian M. Does branchiogenic carcinoma really exist? Arch Pathol Lab Med. 1976;100:311-314. 10. Bernstein A, Scardino PT, Tomaszewski MM, Cohen MH. Carcinoma arising in a branchial cleft cyst. Cancer. 1976;37:2417-2422. 11. McCarthy SA, Turnbull FM. The controversy of branchiogenic carcinoma. Arch Otolaryngol. 1981;107:570-572. 12. Browder JP, Wheeler MS, Henley JT, Geratz JD. Mucoepidermoid carcinoma in a cervical cyst: a case of branchiogenic carcinoma? Laryngoscope. 1984;94:107-112. 13. Sandiford JA, Chun BK, Potter JF. Branchiogenic carcinoma. J R Coll Surg Edinb. 1987;32:148-151. 14. Soderstgrom K. In situ carcinoma in branchial cyst. ORL J Otorhinolaryngol Relat Spec. 1987;49:149-151. 15. Karmody CS. A classification of the anomalies of the first branchial groove. Otolaryngol Head Neck Surg. 1979;87:334-338. 16. Gerber D, Hugo NE. Branchial cleft cyst in parotid gland. Ann Plast Surg. 1982;9:413-414. 17. Krogdahl AS. Carcinoma occurring in branchial cleft cysts. Acta Otolaryngol. 1979;88:289-295.
Downloaded From: http://archotol.jamanetwork.com/ by a University of Pennsylvania User on 05/14/2015
S.
Park, MD, Collin S. Karmody,
Primary branchiogenic carcinoma was previously a deentity. Initially it was a popular diagnosis for many carcinomas of the neck. Then, in 1950, stringent cricystic teria were defined for establishing the diagnosis of primary branchiogenic carcinoma. Only a limited number of cases have successfully fulfilled these criteria. We describe a pa\s=b\
bated
tient who meets the criteria and who we believe represents the first reported case of a carcinoma arising from the vestigium of the first branchial cleft. We also review the literature on branchial cleft carcinomas and discuss the diagnosis, histopathologic features, and therapeutic options. (Arch Otolaryngol Head Neck Surg. 1992;118:969-971)
than 100 years ago, Von Volkman1 claimed that had arisen from the epithelial lining of Morecarcinoma of the branchial He three a a
apparatus. reported vestigium cases of cystic, squamous cell carcinoma in the neck that had not arisen from any obvious primary lesions and sug¬ gested that they were neoplasms of branchial cleft origin. The diagnosis of primary branchial cleft carcinoma (BCC) quickly gained popularity. About 50 years and 250 cases of
BCC later, Martin et al2 reviewed the literature and concluded that such a diagnosis, however convenient, was premature and inaccurate. In fact, they argued that only three reports, by Oliver,3 provided reasonable evidence for carcinomas arising from branchial arch vestigia. Martin and colleagues argued that lengthy disease-free survival is pivotal in order to rule out the late appearance of a primary focus of tumor of the upper aerodigestive tract. Five-year tumor-free survival is believed to provide "reasonable" evidence that no occult primary tumor exists. Martin and coworkers established four criteria to be fulfilled in order to establish a diagnosis of BCC: (1) the tumor should oc¬ cur where branchial clefts are found, ie, along a line from the tragus, down the anterior border of the sternocleido¬ mastoid muscle, to the clavicle; (2) the histologie appear¬ ance of the lesion should be consistent with tissue known to be present in branchial vestigia; (3) the patient must survive for 5 years with consistent examinations and no evidence of a primary focus; and (4) there should be his¬ tologie proof that the carcinoma arises directly from nor¬ mal cyst epithelium. The fourth criterion is thought to be
Accepted for publication June 2, 1992. From the Department of Otolaryngology, New England Medical Cen-
ter, Tufts University School of Medicine, Boston, Mass. Reprint requests to New England Medical Center, PO Box 850, 750
Washington St, Boston,
MA 02111 (Dr
Karmody).
MD
sine qua non for the diagnosis of BCC. With that in mind, Martin and colleagues concluded that no cases to date were definitive proof of the existence of a carcinoma of bran¬
chiogenic origin.
Since 1950 there have been a limited number of case
re¬
ports in which it was stated that the carcinomas originated from the epithelial lining of branchial cysts, and fewer still
that satisfy Martin and coworkers'2 criteria.4"14 All the pub¬ lished cases describe an epidermoid carcinoma in the re¬ gion of the second branchial apparatus. We describe another patient who satisfies Martin and colleagues' crite¬ ria and who we believe represents the first case of carcinoma arising from the first branchial vestigium. REPORT OF A CASE A 23-year-old woman presented with a 5-month history of in¬ tractable pain in the right preauricular area. The pain was dull, radiated to the face, and was not exacerbated by mastication. The patient denied prior trauma, otorrhea, hearing loss, dysphagia, and hoarseness. She had been treated elsewhere with antibiotics for otitis externa and with intermaxillary wiring for temporo¬ mandibular joint dysfunction. She had a 3-pack-year history of smoking and drank alcohol only occasionally. On examination there was a subtle fullness in the area of the right parotid gland, with moderate tenderness and mild trismus. Her neck, tympanic membrane, oral cavity, and pharynx were normal. The external auditory canal revealed a small pit on the anterior floor of the meatal skin, to which a probe could be passed to 1 cm. No puru¬ lence could be expressed from either the pit or Stensen's duct. All cranial nerves were intact. The diagnosis was an infected first branchial cleft duplication anomaly, and intravenous antibiotic therapy was initiated. After 5 days there was no clinical improve¬ ment. A computed tomographic scan then revealed a smooth, circular lucency in the deeper right parotid gland (Fig 1). Surgi¬ cal excision was recommended, and after consenting to the pro¬ cedure, the patient was taken to the surgical suite, where the right parotid gland was explored via the usual approach. Intraopera¬ tively a lxl-cm firm mass was found immediately deep to the facial nerve, clearly involving the buccal branch. There was a tract extending from the cyst toward the ear canal. The patient under¬ went a total parotidectomy with sacrifice of the buccal division. A postoperative facial paresis eventually resolved, and the patient was relieved of the facial pain. The final pathologic diagnosis was invasive squamous cell carcinoma arising from a first branchial cleft cyst. She received postoperative radiation therapy (65 Gy) to the right parotid bed and now, 7 years later, is doing well and is free of tumor.
PATHOLOGIC FINDINGS the lesion was an encapsulated cyst within pa¬ Grossly rotid tissue. Histologically there was a nonspecific chronic
Downloaded From: http://archotol.jamanetwork.com/ by a University of Pennsylvania User on 05/14/2015
Fig 3.—Photomicrograph showing the benign stratified squamous epi¬ thelium with keratin debris (hematoxyling-eosin, original magnification XI00).
Fig 1.—Axial-image computed tomogram showing lucent lesion deep right parotid gland.
in
the
Fig 4.—Invasive squamous cell carcinoma shown to evolve directly from neighboring benign epithelium (hematoxylin-eosin, original magnifica¬ tion X100).
Fig 2.—Low-power photomicrograph demonstrating the cystic nature of the
parotid lesion (hematoxylin-eosin, original magnification X40).
sialadenitis with acinar atrophy and a cystic structure con¬ taining keratin debris (Fig 2). The cyst was lined with benign, keratinizing stratified squamous epithelium (Fig 3). In some foci, however, this benign epithelium was observed to evolve directly into an infiltrating, well-differentiated squamous cell carcinoma (Fig 4). Local inflammation sur¬ rounded the invading tumor edge. There was soft-tissue ex¬ tension as well as intraneural and perineural infiltration by rumor
(Fig 5).
COMMENT Anomalies of the first branchial cleft are categorized into four variants: (1) aplasia, (2) atresia, (3) stenosis, and (4) du¬ The duplication anomaly is found in two forms, plication.15 and 1 type 2. They both have a well-formed external au¬ type 1 ditory canal, but in addition there is a second tract. Type is a duplication of the membranous canal and
Fig 5.—Neural tissue containing metastaticXsquamous (hematoxylin-eosin, original magnification 100).
Downloaded From: http://archotol.jamanetwork.com/ by a University of Pennsylvania User on 05/14/2015
cell carcinoma
usually is found either anterior or posterior to the pinna, running parallel to the canal until exiting in the medial ca¬ nal or, rarely, in the middle ear space. Type 2 is a dupli¬ cation of the membranous canal and is composed of ecto¬ derm and mesoderm, running from the infra-auricular area superiorly toward the canal. It frequently courses deep within the parotid gland and may interwind between
the branches of the facial nerve. Both types are rare clini¬ cal findings, with only about 50 reported cases.16 The incomplete obliteration of any branchial tract will result in a sinus or cyst. The cyst is lined with an epidermal derivative, usually stratified squamous epi¬ thelium. It is possible for carcinomatous degeneration of the cyst lining to occur. However, it is unreasonable to assume such a diagnosis based merely on the finding of a cystic, cervical carcinoma without a primary focus of tumor. The controversy arises from the facts that (1) the jugular lymphatics and most branchial cysts are found in similar regions; (2) metastic squamous carcinoma is expected to occur with far greater frequency than a primary branchiogenic carcinoma; (3) a cervical metasta¬ sis may be the presentation of an occult lesion that only later presents itself in the upper aerodigestive tract; and (4) histologically it is difficult to distinguish a BCC from the cystic degeneration of a metastatic cervical node. Krogdahl17 made histologie comparisons between 154 branchial cleft cysts and normal lymph nodes. She de¬ scribed several characteristics that they share, but she also noted three features that are exclusive to lymph nodes: peripheral lobulation, internodular trabeculae, and perinodular sinuses. There is clinical relevance in distinguishing BCC from metastatic squamous cell car¬ cinoma in that careless reassurance, therapeutic compla¬ cency, and needless overtreatment are all to be avoided. A patient must survive tumor free for 5 years to fulfill the third criterion of Martin et al.2 Therapeutic decisions are made at the time of diagnosis, however, not after the 5-year requirement is satisfied. Postoperative radia¬ tion therapy is used to extirpate residual microscopic disease. This treatment option extends to the squamous carcinomas of branchiogenic origin. When a patient pre¬ sents with a cystic, squamous cell carcinoma, potentially of branchiogenic origin, oncologie excision followed by
is a sound therapeutic option. Our patient represents another case of branchiogenic carcinoma and we believe is the first one reported to have such a lesion of the first branchial apparatus. She had a type 1 duplication anomaly of the first branchial cleft with carcinomatous degeneration arising directly from normal squamous epithelium, and she fulfilled the criteria estab¬ lished by Martin and colleagues. The nonspecific sialad¬ enitis and perineural invasion presumably accounted for her pain. Postoperative radiotherapy was elected because a radical oncologie excision was not possible without mas¬ sive disfigurement. Our patient remains disease free 7 years after her initial presentation.
radiotherapy
References 1. Von Volkmann R. Das tiefe branchiogege Halskarcinom. Zentralbl Chir.
1882;9:49-63. 2. Martin H, Morfit HM, Erlich H. The case for branchiogenic cancer (malignant brachioma). Ann Surg. 1950;132:867-887. 3. Oliver RL. Malignant epithelial tumors of the neck: carcinoma of branchiogenic origin. Am J Cancer. 1935;23:16. 4. Hill FT, Goodof II. Branchiogenic carcinoma. Ann Otol Rhinol Laryngol. 1952;61:474-482. 5. Stackpole RH, Pearce JM. Branchial cleft carcinoma. Arch Surg. 1961; 82:347-352. 6. Schuring A, Arthur J. Branchiogenic carcinoma does exist. Throat Mon. 1967;46:752-753. 7. Katubig C, Damjanov I. Branchial cleft carcinoma. Arch
Eye Ear Nose
Otolaryngol.
1969;89:92-93. 8. Benisch BM, Som ML. Branchial cleft carcinoma. Arch Otolaryngol. 1973;98:208-209. 9. Compagno J, Hyams VJ, Safavian M. Does branchiogenic carcinoma really exist? Arch Pathol Lab Med. 1976;100:311-314. 10. Bernstein A, Scardino PT, Tomaszewski MM, Cohen MH. Carcinoma arising in a branchial cleft cyst. Cancer. 1976;37:2417-2422. 11. McCarthy SA, Turnbull FM. The controversy of branchiogenic carcinoma. Arch Otolaryngol. 1981;107:570-572. 12. Browder JP, Wheeler MS, Henley JT, Geratz JD. Mucoepidermoid carcinoma in a cervical cyst: a case of branchiogenic carcinoma? Laryngoscope. 1984;94:107-112. 13. Sandiford JA, Chun BK, Potter JF. Branchiogenic carcinoma. J R Coll Surg Edinb. 1987;32:148-151. 14. Soderstgrom K. In situ carcinoma in branchial cyst. ORL J Otorhinolaryngol Relat Spec. 1987;49:149-151. 15. Karmody CS. A classification of the anomalies of the first branchial groove. Otolaryngol Head Neck Surg. 1979;87:334-338. 16. Gerber D, Hugo NE. Branchial cleft cyst in parotid gland. Ann Plast Surg. 1982;9:413-414. 17. Krogdahl AS. Carcinoma occurring in branchial cleft cysts. Acta Otolaryngol. 1979;88:289-295.
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