PEDIATRIC SUBMANDIBULAR TRIANGLE MASSES: A FIFTEEN-YEAR EXPERIENCE
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1 PEDIATRIC SUBMANDIBULAR TRIANGLE MASSES: A FIFTEEN-YEAR EXPERIENCE Neil G. Hockstein, MD, 1 Daniel S. Samadi, MD, 1 Kristin Gendron, MD, 1 David Carpentieri, MD, 2 Ralph F. Wetmore, MD 1 1 Division of Pediatric Otolaryngology, Children s Hospital of Philadelphia, The University of Pennsylvania School of Medicine, One Wood Building, Philadelphia, Pennsylvania wetmore@ .chop.edu 2 Department of Pathology, Children s Hospital of Philadelphia, The University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania Accepted 21 January 2004 Published online 12 May 2004 in Wiley InterScience ( DOI: /hed Abstract: Background. The purpose of this study was to evaluate the surgical results of pediatric submandibular triangle masses, with specific attention to neoplastic processes. Methods. We retrospectively reviewed the medical records of 105 patients aged 6 months to 21 years who underwent surgery in the submandibular triangle at a major pediatric tertiary care hospital from 1987 to Results. One hundred five patients who underwent surgery in the submandibular triangle were included in the study. Twenty patients had neoplastic processes, six of which were of primary salivary origin (two mucoepidermoid carcinomas and four pleomorphic adenomas). Twenty-four patients underwent excision of inflamed or infected lymph nodes, and 23 patients underwent excision of inflamed or infected submandibular glands. Thirty-eight patients were included who underwent surgery for sialorrhea or to gain access for another surgical procedure. Complications included tumor recurrence, transient and permanent marginal mandibular nerve weakness, ranula, postoperative fluid collection, and cellulitis. Duration of follow-up ranged from no follow-up to 11 years. Conclusion. Surgical excision of submandibular triangle masses is uncommon. We present our experience with these lesions, with a discussion of diagnosis, surgical indications, and surgical complications. A 2004 Wiley Periodicals, Inc. Head Neck 26: , 2004 Correspondence to: Ralph F. Wetmore Presented at the Annual Meeting of the American Society of Pediatric Otolaryngology, Inc., May 13 14, 2002, Boca Raton, Florida B 2004 Wiley Periodicals, Inc. Keywords: pediatric submandibular mass; neoplastic process; surgery; excision Disease within the submandibular triangle in children that requires surgery is uncommon. Most pediatric submandibular triangle lesions are inflammatory and resolve spontaneously or with a short course of antibiotics. Infrequently, the lesions persist and surgical excision is performed, either for treatment or diagnostic purposes. Neoplastic lesions may arise from any of the structures that occupy this anatomic locale that is bounded by the inferior border of the mandible and the anterior and posterior bellies of the digastric muscle. The submandibular triangle houses glandular, vascular, nervous, and lymphatic tissues. As a result of the variety of tissue types, many different tumors may be found, although none occurs with any great frequency. PATIENTS AND METHODS We retrospectively reviewed the medical records of all patients under 21 years of age who underwent surgical excision of any structure within the submandibular triangle at the Children s Hospital of Pediatric Submandibular Masses HEAD & NECK August
2 Philadelphia between May 11, 1987, and July 11, 200l. Patients who underwent surgery in the submandibular triangle as part of a larger resection were also included in the data set. The clinical history, surgical procedure, histopathologic findings, and postoperative course were reviewed. Pathologic specimens from 105 patients included tissue from the submandibular triangle. On the basis of the pathologic diagnosis, patients were categorized into four groups. Group I included patients with neoplastic diseases found within the submandibular triangle. Group II was composed of patients with submandibular triangle lymph nodes that were either infected or inflamed. Group III included patients whose submandibular glands were either infected or inflamed. Group IV included 35 patients who underwent bilateral submandibular gland excision for the treatment of sialorrhea and three patients who underwent excision of the submandibular gland to gain access for another surgical procedure. These 38 patients (73 surgical sides) were included in the study solely for the assessment of marginal mandibular nerve injury. RESULTS The 105 patients included in the study included 52 boys (50%) and 53 girls (50%). The average age F standard deviation (SD) was 10.9 years F 6.2 years (range, 0.5 to 20.6 years). Group I, the neoplastic group, included 20 (30%) of the 67 patients with submandibular triangle masses (Table 1). Nine (45%) of these Diagnosis Table 1. Group I Neoplasia. No. patients Mean age, y Complications* Pleomorphic adenoma Recurrence and mild nerve weakness (1) Mucoepidermoid Recurrence (2) carcinoma Transient nerve weakness (1) Lymphangioma Nerve weakness (1) Nerve sacrifice (1) Fluid collection 3 (1) Hemangioma None Hodgkin s None disease PTLD None Desmoid fibromatosis None Abbreviation: PTLD, post-transplant lymphoproliferative disorder. *Numbers in parentheses represent number of patients with each complication. patients were male, and 11 (55%) were female; the average age was 11.5 years. Six (30%) of these lesions were of primary salivary origin, and 14 (70%) were derived from other tissues. Of the salivary lesions, four were pleomorphic adenomas and two were mucoepidermoid carcinomas. Three of the four patients with pleomorphic adenomas suffered no complications. One patient suffered a recurrence and underwent reexcision. This patient suffered mild weakness of the marginal mandibular nerve. Both patients who had mucoepidermoid carcinomas were initially treated with partial excision at outside hospitals and both eventually developed recurrences, which were later completely resected at our institution. One patient had transient weakness of the marginal mandibular nerve. One of the two patients was treated with a modified radical neck dissection for cervical metastasis as well as with radiation therapy. His disease is controlled as of 11 years follow-up. The average length of follow-up was 3.8 years for patients with primary salivary neoplasms. Of the 14 patients with neoplastic processes of nonsalivary origin, six (43%) of these patients had lymphangioma that infiltrated the submandibular triangle. In all cases, the lymphangioma was diagnosed preoperatively by imaging including CT, MRI, and ultrasound (US); complete imaging results (copy of report of films) were available for four patients. The average age of this group at the time of excision was 6.3 years. Two patients suffered weakness of the marginal mandibular nerve. In one of these patients, the facial nerve was knowingly sacrificed because it could not be identified in the large tumor mass. It was reconstructed with a fascial sling. One patient postoperatively developed a fluid collection, which required surgical drainage on three occasions. Diagnosis Table 2. Group II Submandibular lymph nodes. Reactive lymphadenopathy Cat scratch disease Atypical mycobacteria Necrotizing lymphadenitis No. patients Mean age, y None None Complications* Recurrence 2 (1) None *Number in parentheses represents number of patients with each complication. 676 Pediatric Submandibular Masses HEAD & NECK August 2004
3 Diagnosis Table 3. Group III Submandibular gland with inflammatory disease. No. patients Mean age, y Complications* Sialadenitis Transient nerve weakness (2) Cellulitis (1) Necrotizing Transient nerve weakness (1) granuloma Sialocele Transient nerve weakness (1) Recurrence (1) Ranula (1) *Numbers in parentheses represent number of patients with each complication. One patient had a hemangioma that was completely excised. Excision of the hemangioma was undertaken because CT demonstated a lytic expansile mass anterior to the mandible, suspected initially to be a soft tissue sarcoma. Two patients who presented with cervical lymphadenopathy were diagnosed with Hodgkin s disease. Three patients with histories of organ transplantation (two liver, one lung) who were on chronic immunosuppressive therapy were diagnosed with post-transplant lymphoproliferative disorder (PTLD). Finally, two patients with known desmoid fibromatosis had tumors within the submandibular gland that were excicised en bloc with the tumor. Of the 20 patients with neoplastic processes involving the submandibular triangle, only two (10%) suffered permanent nerve weakness that was not the result of intentional nerve sacrifice (one pleomorphic adenoma and one lymphangioma). Group II included 24 patients who underwent submandibular lymph node excision (Table 2). There were twelve boys (50%) and 12 girls (50%). The average age F SD was 9.8 F 5.7 years. In Table 4. Radiographic findings. Diagnosis Imaging modality Result Lymphangioma CT/US Low-density 5.5-cm greatest diameter complex collection Lymphangioma MRI Complex cystic collection, heterogeneous signal intensity Lymphangioma MRI Complex neck mass, heterogeneous signal intensity Lymphangioma CT Multiloculated cystic mass consistent with cystic hygroma Pleomorphic adenoma MRI cm well-circumscribed mass Pleomorphic adenoma CT R submandibular mass, likely necrotic lymph node Pleomorphic adenoma MRI R submandibular mass with multiple subcentimeter nodes, favor tumor Hodgkin s lymphoma CT L submandibular mass, lymphadenopathy vs submandibular gland mass PTLD CT Shotty lymphadenopathy with multiple nodes up to 1 cm PTLD CT L submandibular node, <1 cm; increased size from prior study Hemangioma CT Lytic expansile mass anterior to L mandible, suspect sarcoma Lymphoid hyperplasia US Cystic lesion inferior to right mandible, suspect branchial cleft cyst Reactive lymph node CT Nodule anteroinferior to R submandibular gland, likely reactive node Reactive lymph node CT/MRI L submandibular mass suspicious of lymphoma Reactive lymph node MRI R submandibular mass lymph node vs lymphoma vs rhabdomyosarcoma Necrotizing lymphadenitis CT/MRI Mass posterior to R mandible likely necrotic lymph nodes (MRI: likely inflammatory node) Atypical mycobacteria MRI Likely inflammatory lymph nodes Necrotizing granuloma CT cm lesion lateral to R submandibular gland extending to skin consistent with atypical mycobacteria Sialadenitis CT Mildly enlarged R submandibular gland with calcifications Sialadenitis MRI Shotty lymphadenopathy, submandibular glands normal-appearing Sialadenitis MRI Bilateral L>R multicystic septated lesions with enhancement suggestive of lymphangioma or atypical plunging ranula Sialadenitis CT Necrotic, heterogeneously enhancing R submandibular mass extending into overlying subcutaneous tissue Caseating granuloma CT Shotty bilateral posterior cervical lymphadenopathy, otherwise normal Sialadenitis X-ray No salivary masses or calculi Sialadenitis MRI 5-cm rim-enhancing cystic structure L floor of mouth Submandibular abscess CT cm L submandibular mass with areas of low attenuation Sialadenitis CT Normal submandibular glands Sialadenitis MRI Enlarged anterolateral neck mass/submandibular gland, suspect lymphangioma Abbreviations: R, right; L, left; PTLD, post-transplant lymphoproliferative disorder. Pediatric Submandibular Masses HEAD & NECK August
4 12 cases, histopathologic examination demonstrated reactive lymphadenopathy. None of these patients suffered any surgical complications. Of the remaining 12 patients, two had cat scratch disease, three had culture-positive atypical mycobacteria, and seven had necrotizing lymphadenitis without microbiologic identification. The negative cultures were likely due to preoperative antibiotic therapy. One patient with atypical mycobacteria suffered two recurrences. No patients suffered nerve weakness. Group III included 23 patients who underwent excision of their submandibular gland for inflammatory disease (Table 3). Twelve (52%) were boys, and 11 (48%) were girls. Sixteen patients (70%) had sialadenitis, four (17%) had necrotizing granulomas within their submandibular gland, and three (13%) had a sialocele. Four patients suffered transient weakness of the marginal mandibular nerve that lasted less than 2 weeks. Two of these patients had sialadenitis, one had a sialocele, and one a necrotizing granuloma. One patient with a sialocele suffered a recurrence, which was later completely re-excised. One patient developed a ranula and underwent marupialization and excision of the sublingual gland. One patient developed a mild cellulitis around the incision. Group IV included 35 patients with chronic sialorrhea who underwent bilateral submandibular gland excision and three patients who underwent excision of the submandibular gland and surrounding structures to gain access for another surgical procedure. Among these 73 surgical sides, there were no nerve injuries. Complete radiographic data, either an official report or the actual scan, were available for 28 patients of the patients from groups I, II, and III (42%). Incomplete data were available for the remaining patients. Radiographic findings are presented Table 4. Of patients with tumors, two were misdiagnosed radiographically. The patient with the hemangioma had a CT scan which was read as suspicious for a sarcoma (Ewing s) due to erosion of the mandible. One patient with a pleomorphic adenoma had CT findings that were interpreted as a necrotic lymph node; the patient underwent excision and is disease-free at 2 years follow-up. DISCUSSION Fewer than 5% of all salivary tumors occur in children. When salivary tumors do occur in children, they are approximately 10 times more likely to occur in the parotid gland than the submandibular gland A study of 9993 salivary gland lesions examined at the Armed Forces Institute of Pathology (AFIP) revealed only 10 cases of pleomorphic adenoma and four cases of mucoepidermoid carcinoma of the submandibular gland in children. 14 In the AFIP study, the largest reported series, submandibular tumors do not demonstrate a predilection for sex. 14 Most commonly, masses in the submandibular triangle represent an inflammatory lesion or a lesion of vascular origin. Historically, as in our study, submandibular gland excision is most frequently performed for chronic sialadenitis. 15,16 Because of the high incidence of submandibular gland calculi, sialadenitis of the gland is not uncommon. 17 Vascular proliferative lesions, such as hemangiomas and lymphatic malformations (lymphangiomas), may be the most common masses in the submandibular triangle (>50%). 1,4,18 In our series, we report only one case of a hemangioma. This underrepresentation is due to the infrequency in which these lesions require excision or biopsy. Diagnosis by contrast-enhanced MRI precludes the need for biopsy. Typically, hemangiomas involute, and only when they interfere with feeding or respiration do we recommend excision. Differential diagnosis of infectious lesions in the submandibular triangle must include bacterial and mycobacterial pathogens. The most common bacterial organisms include Staphylococcus and Streptococcus species as well as Haemophilus influenza and, less commonly, anaerobic and gram-negative organisms. Atypical mycobacteria must also be considered in the differential diagnosis. Atypical mycobacterial organisms include Mycobacterium avium, Mycobacterium avium-intracellulare, Mycobacterium malmoense, Mycobacterium bovis, and Mycobacterium scrofulaceum. 19 On physical examination, it is difficult to differentiate bacterial infection from mycobacterial infection. Skin testing is often nondiagnostic for atypical mycobacterial infection, and a tissue specimen is frequently required for definitive diagnosis. Atypical mycobacterial infection in adults is typically treated with either fluoroquinolones or macrolides, but in the pediatric population, fluoroquinolones are contraindicated. In both children and adults, dual antibiotic therapy with clarithromycin and rifampin may be considered, but even with appropriate antibiotic therapy, mycobacterial infection may require surgical excision in close to 90% of cases. Treatment options for infectious lesions refrac- 678 Pediatric Submandibular Masses HEAD & NECK August 2004
5 tory to medication therapy include excision or curettage. We typically perform excision and feel that it allows more complete exenteration of infection with preservation of vital structures. Approximately 50% of submandibular tumors are benign. 3,7 The incidence of malignancy in submandibular tumors is 2 to 3 times that of parotid tumors. In children, malignant tumors are rare, and when they do occur, they are typically found in older children. 23 The two patients in our study with primary salivary malignancies presented at 11 years of age. In adults, adenoid cystic carcinoma is the most common submandibular tumor, but it is infrequently seen in children. 3,7,14,24 Oncocytoma and Warthin s tumor are also rarely seen in children. 3,14 In the pediatric population, mucoepidermoid carcinoma is the most frequent malignant tumor, and patients suffer recurrence or metastasis in 30% to more than 50% of cases. 1,25,26 With surgery alone, these recurrence rates are unacceptable. Radiation therapy, when indicated, has been reported to increase control rates to 88% at 10 years. 27 Overall, patients with submandibular malignancies fare worse than do those with malignant parotid tumors. 28 In addition to the rare primary salivary cancers of the submandibular triangle, other malignant tumors may present in this anatomic region. In patients with diffuse cervical lymphadenopathy and a suspected diagnosis of lymphoma, surgeons tend to avoid biopsy in the submandibular triangle to avoid damage to the marginal mandibular nerve. We report two cases of Hodgkin s lymphoma that presented as a submandibular triangle mass. We also identified three patients with PTLD at our institution, which has a very busy oncology service; these lesions may be overrepresented in our study. In patients on chronic immunosuppressive therapy, a high index of suspicion must be maintained to diagnose this disease. The dilemma faced by many surgeons is how to identify patients with submandibular masses that require surgery and to define the scope of surgery that is required. At our institution, we seldom used fine-needle aspiration cytology (FNAC) during the years the patients in this study were treated. FNAC has become the standard of care in adults, with sensitivity and specificity for submandibular triangle masses in adults reported to be greater than 90% at experienced institutions. 17,24 Data regarding FNAC for diagnosis of pediatric salivary masses are still sparse. Several small series report similar sensitivity and specificity in children, but FNAC requires a patient who is able to tolerate the procedure as well as an experienced cytopathologist. 29,30 Further study of the role of FNAC in children is warranted; it promises to aid in identifying patients with neoplastic lesions. Our treatment algorithm starts with a trial of antibiotics aimed at Staphylococcus sp., Streptococcus sp., and H. influenza for any lesion suspected to be of inflammatory origin. Submandibular triangle tumors that affect children may frequently behave like nonneoplastic lesions. Because submandibular triangle malignancy is so rare in the pediatric population and the tumors are often slow growing, little is lost by starting treatment with antibiotic therapy. We typically use an aminopenicillin with a h-lactamase inhibitor (amoxicillin/clavulinic acid or ampicillin/sulbactam). Lesions that appear to be inflammatory that do not initially respond to antibiotic therapy may be treated with an extended course or with a different agent (vancomycin or a macrolide). For lesions that are not clearly inflammatory that persist despite a 2-week course of appropriate antibiotic therapy, imaging studies including MRI, CT, and US may be performed. Solid, ie, nonvascular, lesions are then excised using oncologic principles. Infrequently, frozen section diagnosis is employed in our surgical decisionmaking process. With an incorrect intraoperative diagnosis, local control is compromised because an inadequate operation may be performed. Our data, as demonstrated in two patients with mucoepidermoid carcinoma incompletely excised at outside hospitals, corroborate the historical experience of poor local control rates seen with this tumor. Perhaps the most feared complication of surgery in the submandibular triangle is damage to the marginal mandibular branch of the facial nerve. Additionally, the lingual and hypoglossal nerves may be damaged, although much less commonly. Nerve damage may be caused by transection, stretch or crush injury, thermal injury from electrocautery, or ischemic injury from aggressive dissection of the nerve. Three techniques of protecting the marginal mandibular nerve have been described: (1) direct identification and dissection of the nerve, (2) low division of the facial vessels, and (3) a low nonidentification approach. 31,32 Low division of the facial vessels retracts the marginal mandibular nerve superiorly, thus removing it from the surgical field. The low nonidentification relies on the nerve not coursing more than 2 cm inferior to the mandible Pediatric Submandibular Masses HEAD & NECK August
6 and lying in a plane deep to the platysma but superficial to the fascia overlying the submandibular gland, thus elevating the fascia overlying the submandibular gland at this level protects the nerve. In a series by Ichimura et al 31 using the low nonidentification approach, nerve weakness occurred in 18.2% of patients. Reports of the incidence of nerve injury range from 0% to approximately 50%. 15,31,32 In our series, using the low nonidentification technique five patients (4%) suffered transient paresis of the marginal mandibular nerve. Permanent weakness occurred in three patients (2%), two with large lymphangiomas (one nerve was intentionally sacrificed) and one with a recurrent pleomorphic adenoma. Our data with respect to nerve injury correspond to data in other reported series. CONCLUSION Tumors of the submandibular triangle in children are exceedingly rare. Most frequently, submandibular triangle masses in children are inflammatory in nature. Unfortunately, if misdiagnosed, submandibular tumors may be incompletely excised and thus lead to unacceptable recurrence rates. We recommend using a low nonidentification approach to the marginal mandibular nerve and recommend treating all cases in which the diagnosis of neoplasm cannot be excluded as such. By using oncologic surgical principles, recurrence rates can be decreased without sacrificing marginal mandibular nerve function. REFERENCES 1. Bentz BG, Hughes CA, Ludemaan JP, Maddalozzo J. Masses of the salivary gland region in children. Arch Otolaryngol Head Neck Surg 2000;126: Malone B, Baker SR. Benign pleomorphic adenomas in children. Ann Otol Rhinol Laryngol 1984;93: Eneroth CM. Salivary gland tumors in the parotid gland, submandibular gland, and the palate region. Cancer 1971; 27: Schuller DE, McCabe BF. The firm salivary mass in children. Laryngoscope 1977;87: Rogers DA, et al. Primary malignancy of the salivary gland in children. J Pediatr Surg 1994;29: Byars LT, Ackerman LV, Peacock E. Tumors of salivary origin in children: a clinical pathological appraisal of 24 cases. Ann Surg 1957;146: Skolnik EM, Friedman M, Becker S, Sisson GA, Keyes GA. Tumors of the major salivary glands. Laryngoscope 1977; 87: Bianchi A, Cudmore RE. Salivary gland tumors in children. J Pediatr Surg 1978;13: Castro EB, Huvos AG, Strong EW, Foote FW Jr. Tumors of the major salivary glands in children. Cancer 1972;29: Seifert G, Okabe H, Caselitz J. Epithelial salivary gland tumors in children and adolescents. Analysis of 80 cases (Salivary Gland Register ). J Otorhinolaryngol Relat Spec 1986;48: Spiro RH. The management of salivary neoplasms: an overview. Auris Nasus Larynx 1985;12(Suppl 2): S122 S Rollins L III, Rollins L Jr. Tumors of the salivary glands. Am Surg 1979;45: Greer RO, Mierau GW, Favara BE. Tumors of the head and neck in children. New York: Praeger Publishers; p Krolls SO, Trodahl JN, Boyers RC. Salivary gland lesions in children. Cancer 1972;30: Milton CM, Thomas BM, Bickerton RC. Morbidity study of submandibular gland excision. Ann R Coll Surg Engl 1986;68: Ellies M, Laskawi R, Arglebe C, Schott A. Surgical management of nonneoplastic diseases of the submandibular gland. A follow-up study. Int J Oral Maxillofac Surg 1996; 25: Goh YH, Sethi DS. Submandibular gland excision: a five year review. J Laryngol Otol 1998;112: Martin VT, Salmaso R, Onnis GL. Tumors of salivary glands. Review of 479 cases with particular reference to histological types, site, age, and sex distribution. Appl Pathol 1989;7: Cox HJ, Brightwell AP, Riordan T. Non-tuberculosis mycobacterial infections presenting as salivary gland masses in children: investigation and surgical management. J Laryngol Otol 1995;109: Jervis PN, Lee JA, Bull PD. Management of non-tuberculous mycobacterial peri-sialadenitis in children: the Sheffield otolaryngology experience. Clin Otolaryngol Allied Sci 2001;26: Hazra R, Robson CD, Perez-Atayde AR, Husson RN. Lymphadenitis due to nontuberculous mycobacteria in children: presentation and response to therapy. Clin Infect Dis 1999;28: Ghebremichael S, Svenson SP, Kallenius G, Hoffner SE. Antimycobacterial synergism of clarithromycin and rifabutin. Scand J Infect Dis 1996;28: Baker SR, Malone B. Salivary gland malignancies in children. Cancer 1985;55: Camilleri IG, et al. Malignant tumours of the submandibular salivary gland: a 15-year review. Br J Plast Surg 1998;51: Galich R. Salivary gland neoplasms in childhood. Arch Otolaryngol 1969;89: Pyper PC, Beverland DE, Bell DM. Tumours of the submandibular gland. J R Coll Surg Edinb 1987;32: Storey MR, Garden AS, Morrison WH, Eicher SA, Schechter NR, Ang KK. Postoperative radiotherapy for malignant tumors of the submandibular gland. Int J Radiat Oncol Biol Phys 2001;51: Hocwald E, Korkman H, Yoo GH, et al. Prognostic factors in major salivary gland cancer. Laryngoscope 2001;111: Diament MJ, Stanley P, Taylor S. Percutaneous fine needle biopsy in pediatrics. Pediatr Radiol l985;15: Wakely PE Jr, Kardos TF, Frable WJ. Application of fine needle aspiration biopsy to pediatrics. Hum Pathol l988; 19: Ichimura K, Nibu K, Tanaka T. Nerve paralysis after surgery in the submandibular triangle: review of the University of Tokyo Hospital experience. Head Neck 1997; 19: Hlad J, Andreassen UK. Submandibular gland excision: short- and long-term complications. J Otorhinolaryngol Relat Spec 1994;56: Pediatric Submandibular Masses HEAD & NECK August 2004
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