IMAGING OF GRANULOMATOUS LESIONS OF THE NECK IN CHILDREN

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RADIOLOGIC EVALUATION OF THE NECK

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IMAGING OF GRANULOMATOUS LESIONS OF THE NECK IN CHILDREN Caroline D. Robson, MB, ChB

Granulomatous lesions of the neck are common in children. The granulomatous response is a generic reaction to the presence of a persistent endogenous or exogenous insoluble irritant, which is dependent on the state of the host's immune ~ y s t e m .Granulomatous ~ inflammation is a specific type of chronic inflammation characterized by accumulations of modified macrophages called epithelioid cells. Granulomatous lesions are usually infectious in origin and are classified according to the causative organism as bacterial, fungal, or parasitic in nature. Granulomatous inflammation is one of the more common findings in chronically enlarged, surgically excised lymph nodes in children. In adults tuberculosis (TB), nontuberculous mycobacteria (NTM), sarcoidosis, fungal infections, rheumatoid disease, and foreign body inclusions cause the majority of cases of granulomatous lymphadenitis. Less common causes of granulomatous inflammation include brucellosis, schistosomiasis, syphilis, and leprosy. In children in the United States, NTM infection accounts for most granulomatous lesions of the head and neck.4 Because different organisms (e.g., Mycobacterium tuberculosis and NTM) can cause histologically indistinguishable nodal disease, a thorough history and physical examination are essential diagnostic requirements. Although a pre-

sumptive diagnosis can be made based on clinical features, imaging and histopathologic examination, a definitive diagnosis may prove elusive because special stains and culture may fail to demonstrate the causative agent.4Preoperative imaging is used to evaluate for the extent of mass lesions, to document distortion or narrowing of the airway and vessels, and to delineate osseous involvement. NTM INFECTION Mycobacterial infections are usually separated into TB caused by M . tuberculosis and NTM infection caused by all mycobacterial species other than M . tuberculosis. The most common NTM (or atypical mycobacteria) are M . auium-intracellulare, M . scrofulaceum, M . bovis, and M . kansasii. The term scrofula has been applied to cervical lymphadenitis caused by M . tuberculosis and M . bouis, but is currently used to describe any mycobacterial lymphadeniti~.~~ A wide variety of diseases are caused by NTM, including disseminated infections in immunocompromised patients, pulmonary infections predominantly in adults with underlying lung disease, and lymphadenitis in Is Persistent cervicofacial healthy ~hi1dren.l~.

From the Division of Neuroradiology, Department of Radiology, Children's Hospital; and Harvard Medical School, Boston, Massachusetts

RADIOLOGIC CLINICS OF NORTH AMERICA

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VOLUME 38 NUMBER 5 SEMEMBER 2000

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lymphadenitis is the most common manifestation of N T M infection in children and usually occurs in otherwise healthy children under the age of 5 years (peak age 2 to 4 ears).^,^' It is generally accepted that humans acquire NTM from environmenfal sources and cervical lymphadenitis may result from ingestion of NTM. M. avium or M . intracellulure infection accounts for most cases of NTM lymphadenitis, although geographic variation may occur.4 The clinical manifestations of NTM adenitis are considered characteristic. The disease usually manifests as a slowly enlarging unilateral submandibular or preauricular mass of nodes. Fever or other systemic signs of infection are usually absent.I3 Extranodal extension of caseating material may involve the contiguous subcutaneous fat, an adjacent salivary gland, or the skin. In the absence of effective therapy, the mass typically progresses to liquefaction. There is violaceous discoloration of the overlying skin followed by spontaneous drainage through the skin.I3 The affected region is typically nontender, or minimally tender, and signs of acute inflammation are lacking. A delay in diagnosis is common because most cases are presumed to represent suppurative bacterial adenitis. As a result standard antibiotic therapy is often instituted but fails. Culture, isolation, and identification of the organisms may take an additional 2 to 6 weeks. The duration of symptoms is typically weeks to months before a definitive diagnosis is made. When positive, purified protein derivative skin testing in patients with NTM adenitis is typically only weakly reactive.40The treatment of choice for NTM adenitis is excision of the affected lymph nodes, because incision and drainage may lead to recurrence or sinus tract formation.'! '', 41, 42 It is important to distinguish this condition from bacterial adenitis, which is usually treated with incision and drainage. The laboratory diagnosis of mycobacterial infection involves the use of routine histopathologic stains, acid-fast smears, and mycobacterial cultures. Necrotizing granulomatous inflammation is found with TB and NTM infections, and other granulomatous diseases. Stains for acid-fast bacilli are reportedly positive in only 20% to 50% of patients with positive skin tests and histopathology consistent with NTM infection.4O Culture recovery is reported to be approximately 50% to 80% in most series of patients.', 41, 43, 4.1 In

patients who are culture negative, NTM infection is suggested by the appropriate clinical history, physical examination, and pathologic findings in the absence of a history of exposure to TB or cats. In children with NTM adenitis, contrastenhanced CT (or MR imaging) demonstrates characteristic imaging features.%Adenopathy most commonly arises near the angle of the mandible or within the parotid space (Figs. 1-3). Involvement of the retropharyngeal space is unusual and may simulate a retro34 Contrast-enhanced pharyngeal axial CT typically demonstrates asymmetric cervical lymphadenopathy and contiguous low-density, necrotic, ring-enhancing masses involving the subcutaneous fat and skin (see Fig. 1). Unlike conventional bacterial abscesses, inflammatory stranding of the subcutaneous fat is typically minimal or absent in NTM adenitis (see Fig. 3).34Rarely, absence of cutaneous involvement and moderate stranding of the subcutaneous fat may simulate a bacterial abscess. Punctate calcification has been observed in NTM adenitis.2s,34

TB TB is an unusual cause of cervical lymphadenopathy in children in the United

Figure 1. A 3-year-old girl with nontuberculous rnycobacterial adenitis. Mycobacterium avium infracellulare was cultured following excisional biopsy. Contrast-enhanced axial CT demonstrates heterogeneously enhancing enlarged lymph nodes close to the angle of the mandible (arrow). There is necrotic material extruding from the lymph nodes to involve the subcutaneous fat and skin (arrowhead).There is minimal stranding of the subcutaneous fat.

IMAGING OF GRANULOMATOUS LESIONS OF THE NECK IN CHILDREN

Figure 2. A 2-year-old boy with nontuberculous mycobacterial infection. Mycobacterium avium was cultured following superficial parotidectomy. Contrast-enhanced CT reveals enlargement of the left parotid gland and lymph nodes. There is a low attenuation lesion (arrow) that arises from necrotic intraparotid lymph nodes.

States, and is largely seen in children with AIDS or in immigrants from countries where TB is still a widespread problem.Is TB of the neck usually produces painless bilateral posterior triangle and internal jugu-

Figure 3. A 4-year-old girl with nontuberculous mycobacterial infection. Following excisional biopsy of preauricular and submandibular lymph nodes, acid-fast bacilli were identified. Purified protein derivative skin testing was negative. Coronal FSEIR MR shows two rounded foci of high signal intensity (arrowheads) representing necrotic material involving the subcutaneous fat lateral to the masseter muscle.

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lar adenitis.26Involvement of other regions, however, such as the submental and submandibular nodes, may occur. The larynx, pharynx, and thyroid gland are occasionally infected. Unlike NTM adenitis, TB adenitis tends to occur in association with constitutional symptoms and pulmonary disease.36 The clinical features of TB are varied, however, and can be nonspecific. When TB is suspected, evaluation should begin with chest radiographs, a skin test with purified protein derivative tuberculin, and smears and cultures of appropriate body secretions.26Fine-needle aspiration or excisional biopsy with histologic examination and culture of affected lymph nodes may be required to establish a definite diagnosis. Three stages have been described for the imaging appearance of tuberculous lymphadenitis on CT or MR imaging.I9,27 Early in the course of disease involved lymph nodes display nonspecific homogeneous enhancement on contrast-enhanced CT or MR imaging. This stage corresponds pathologically to a tuberculous granuloma with or without minimal necrosis. Progression of disease results in central necrosis, the most common manifestation of tuberculosis. The presence of a conglomerate nodal mass on CT with central lucency and thick rims of enhancement, and minimally effaced fascia1 planes is suggestive of tuberculous adenitis, especially if the patient has a strongly reactive tuberculosis skin test.31On MR imaging the enhancing areas are of intermediate signal intensity on T1-weighted sequences and are hypointense on T2-weighted sequences corresponding to granulation tissue with inflammation. The nonenhancing areas are relatively hypointense on T1-weighted sequences and are markedly hyperintense on TZ-weighted sequences, corresponding to caseation or necrosis.26A large, low-density mass with a thick, sometimes corrugated rim of peripheral enhancement and obliteration of adjacent soft tissue planes is sometimes referred to as a tuberculous abscess. The third pattern is fibrocalcified nodes that are usually seen in patients who have been treated for TB (Fig. 4). Although calcification of lymph nodes is suggestive of tuberculous adenitis,% it is not specific for the disease. Thickening of the retropharyngeal or prevertebral soft tissues on plain films is usually related to cervical tuberculous osteomyelitis. Retropharyngeal lymphadenitis, however, can result from pharyngeal TB.26Laryngeal

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Figure 4. A 5-year-old boy with tuberculosis. The child was systemically unwell with a cough, cervical lymphadenopathy, left otorrhea and a positive purified protein derivative skin test. Acid-fast bacilli were obtained from sputum and from the left ear. Nonenhanced coronal CT demonstrates punctate calcification within enlarged cervical lymph nodes (arrows). There is opacification within the left middle ear space bulging into the external auditoty meatus (arrowhead).

TB results from pooling of infected secretions in the posterior larynx or from hematogenous dissemination to the anterior larynxz0Laryngeal TB manifests as diffuse bilateral laryngeal thickening with or without a focal mass.26Inadequate treatment of TB can lead to laryngeal stenosis or cricoarytenoid fixation.26 CAT-SCRATCH DISEASE

Cat-scratch disease (CSD) is a relatively common granulomatous disease that affects an estimated 2000 people in the United States each year. CSD occurs worldwide without racial or sexual predilection, and is primarily a disease of children. The causative organism is Barfonella henselae, a gram-negative bacillus.6 The spectrum of diseases caused by Barfonella species has expanded and now includes CSD, bacillary angiomatosis, bacillary peliosis, bacteremia, endocarditis, and trench fever.38 A high percentage of young cats carry €3. henselae, and the cat is probably the healthy vector of disease. Scratches from dogs, rabbits, monkeys, porcupine quills, thorns and wooden splinters, and fish bones or hooks have also been associated with the subsequent development of the disease.16 In the immunocompetent patient self-limited, tender regional adenopathy and a history of primary skin inoculation by a cat scratch characterize CSD.30A nonpruritic ery-

thematous inoculation papule, vesicle, or pustule develops 1 to 2 weeks following a scratch in approximately half of all cases. Healing usually occurs without scarring approximately 1 week later, but the primary lesion may remain apparent for several months. The cardinal feature of the disease is painful subacute granulomatous lymphadenopathy that develops proximal to the primary lesion, 1 to 4 weeks following in~culation.~~. Enlarged nodes are generally 2 to 4 cm in size, but may occasionally reach a diameter of 8 to 10 cm.14 Head and neck lymphadenopathy occurs in one third to half of the cases of CSD with cervical, submandibular, and preauricular nodes most frequently enlarged.39Usually only a single nodal group is involved, although multiple nodes within that group may be enlarged. The enlargement generally resolves over 2 weeks to 3 months, but may persist for up to 2 years. Ten percent to 30% of patients develop nodal suppuration that requires surgical treatment, usually within the first few weeks following the inoculati0n.39 Constitutional symptoms, such as low-grade fever and malaise, occur in approximately half of cases.33CSD is usually a self-limited illness that does not necessarily require antibiotic therapy, but disseminated infection that requires treatment may occur. In immunocompromised patients with HIV or organ transplantation, a systemic infection caused by B. henselae has been described that is characterized by cutaneous proliferative vascular lesions (bacillary angiomatosis), subcutaneous nodules, and osteolytic lesions.2 Lytic bone lesions may resemble Langerhans’ cell histiocyt~sis.~ Parinaud’s oculoglandular syndrome consists of a granulomatous lesion on the conjunctiva of the eye and preauricular adenopathy. This occurs as a result of rubbing the eye after holding a cat. Methods used to diagnose Bartonella-associated infections include histopathologic analysis of biopsy specimens, culture of tissue samples, blood culture, and serology? CSD is not diagnosed on routine histologic sections. Unlike mycobacteria, B. henselae is not acidfast, and a Warthin-Starry silver impregnation stain must be specifically requested to demonstrate the small pleomorphic intracellular gram-negative bacilli. Cultivation of Bartonella is difficult, because the bacteria are extremely fastidious. Polymerase chain reaction-based or immunologic methods for the detection of Bartonella in infected tissues have

IMAGING OF GRANULOMATOUS LESIONS OF THE NECK IN CHILDREN

proved useful.25Severe or persistent cases appear to respond best to antibiotics, such as erythromycin and doxycy~line.~~ Although imaging generally does not play a role in the diagnosis of CSD, contrast-enhanced CT or MR imaging demonstrates the extent of disease. Imaging findings in CSD include enlarged lymph nodes with extensive surrounding edema in the distribution of lymphatic drainage proximal to the site of i n o c ~ l a t i o n This . ~ is seen as conspicuous stranding of the subcutaneous fat in the vicinity of inflamed lymph nodes that is unlike the typical imaging appearance of NTM ade-

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nitisMOn CT, the nodal mass enhances heterogeneously and can contain central low-attenuation foci consistent with necrosis (Fig. 5). Similar findings can be seen on MR imaging. Peripheral enhancement suggestive of abscess formation may also be seen.9This appearance simulates more frequently encountered bacterial infections. TULAREMIA Tularemia is a zoonozis caused by Francisella tularensis, a small gram-negative bacillus.

Figure 5. A 9-year-old boy with cat-scratch disease. The child had been exposed to a kitten. Excisional biopsy of the submandibular nodes revealed necrotizing granulomatous disease. The bartonella titer was positive for Bartonella henselae and B. quintana. A, There are low-attenuation, ring-enhancing, enlarged retropharyngeal lymph nodes (arrows) displacing the left internal carotid artery (arrowhead). B, Stranding of the subcutaneous fat (arrowhead) is associated with a nodal mass (asterisk) at the angle of the mandible. C,There is a low-density ring-enhancing lesion (open arrow) overlying the left sternocleidomastoid muscle, which is swollen (asterisk).

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The disease has been described in Europe, Japan, and all parts of the United States.23The disease is transmitted to humans by direct contact with infected animal material (e.g., from rabbits, hares, or muskrats); by insect bites (e.g., ticks, mosquitoes, or deerflies); by inhalation; or by the oral route (e.g., eating 23 infected rabbit).21, The initial clinical manifestations occur after an incubation period of 2 to 6 days (range 1 to 14 days) and include nonspecific symptoms, such as headache, fever, chills, malaise, and fatigue?’ Depending on the site of invasion and on host response, tularemia can manifest in one of six forms. The most common clinical form is ulceroglandular. This is characterized by a primary skin ulcer and painful regional lymphadenopathy.21A primary ulcer in the mouth, acute purulent or membranous tonsillitis, and cervical lymphadenitis occurs in the oropharyngeal form. Fever and tender adenopathy without a primary ulcer are seen in the glandular form (Fig. 6). Oculoglandular tularemia can develop from conjunctival infection. Typhoidal (gastrointestinal)or pulmonary tularemia can be contracted from ingestion or inhalation. Based on work involving outbreaks in Montana and South Dakota, a mild illness with

fever, cervical lymphadenopathy, and malaise appears to be an important clinical presentation of tularemia in children2”35 The disease is most commonly contracted from tick bites in the head and neck area and typically involves children aged 5 to 9 years (range 2 to 20 years). Lymphadenopathy in tularemia most commonly involves the jugular chain of lymph nodes.36Complications, such as pef-icarditis, pneumonia, and hepatitis, may occur. The diagnosis of tularemia is established by the demonstration of serum tularemia agglutinins, which first appear 2 to 3 weeks after infection. Because atypical lymphocytes and a positive monospot test can occur in tularemia, the disease may be mistaken for infectious mononucleosis if the tularemia agglutination titer is not determined.21Histologic examination of lymph node biopsies reveals a nonspecific chronic granulomatous reaction. Cultures of the pathogen are often difficult because of special growth requirements of the organism. The treatment of tularemia consists of tetracycline or streptomycin, and, in some cases, surgical drainage. Imaging findings in tularemia are nonspecific. In oropharyngeal tularemia, inhomogeneous enhancement of enlarged adenoids and

Figure 6. A 3-year-old boy with glandular tularemia. The parents had found a wood tick on his right occipital scalp 2 weeks earlier. Aspiration of the right occipital lesion yielded Francisella tularensis. The imaging appearance in this case simulated that seen in nontuberculousmycobacterial infection (Fig. 1 and 3). A, Axial contrast-enhanced CT image demonstrates a low-density ring-enhancing lesion in the right occipital subcutaneous tissues consistent with a liquefied right occipital lymph node (arrow). Unlike an acute pyogenic abscess, stranding of the subcutaneous fat is not seen. f3, Contrast-enhanced CT of the neck shows heterogeneous peripheral enhancement around a right neck mass (arrow) that extends to the subcutaneous fat and skin.

IMAGING OF GRANULOMATOUS LESIONS OF THE NECK IN CHILDREN

tonsils and lymphadenitis can mimic infectious mononucleosis or severe streptococcal p h a r y n g i t i ~Enlarged .~~ necrotic lymph nodes in tularemia can be of low attenuation and ring-enhancing on CT. Extrusion of necrotic material to involve the subcutaneous fat and skin can be indistinguishable from NTM infection (see Fig. 6). HISTOPLASMOSIS

Histoplasmosis is the most common endemic respiratory mycosis in the United States, where it is most prevalent in the major river valleys of the central and southern states.1o,22 Histoplasmosis is caused by the fungus Histoplasmosis capsulatum. The fungus is associated with avian droppings and is contracted through inhalation of airborne spores. In most patients the primary infection is asymptomatic and the disease is self-limited. When symptoms do occur, they are generally nonspecific and include fever, cough, and malaise. Disseminated infection can occur from an initial pulmonary infection or from reactivation of a previous focus. Head and neck manifestations are relatively uncommon, although the prevalence may be higher than actually reported.22Histoplasmosis can involve the larynx, tongue, palate, buccal mucosa, and pharynx.48 Presentation as an isolated neck mass is u n ~ s u a l . ~ , ' ~ The diagnosis of histoplasmosis is made on the basis of cultures of the organism from affected tissue or identification of yeast forms stained with periodic acid-Schiff or Gomori's methenamine silver. Serologic testing can also be used. In an endemic area, the histoplasmin skin test may be unreliable as an indicator of acute disease. On CT, histoplasmosis may simulate an abscess with a conglomerate necrotic mass of low-attenuation, ring-enhancing lymph nodes.3,22

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nodes are the most commonly involved peripheral lymph nodes in sarcoidosis. Cervical adenopathy is typically bilateral with mobile, nontender nodes. Involvement of salivary glands is usually bilateral and results in nontender chronic enlargement and xerostomia. Salivary gland enlargement, xerostomia, and keratoconjunctivitis sicca can mimic Sjogren syndrome. Heerfordt's syndrome (uveoparotid fever) refers to acute sarcoidosis manifesting as parotid enlargement, anterior uveitis of the eye, facial paralysis, and fever.R,29 The diagnosis of sarcoidosis is established using a combination of clinical, radiographic, and histopathologic findings and negative special stains and cultures for organisms. Elevated serum angiotensin-converting enzyme levels and documentation of pulmonary involvement strongly support the diagnosis. On CT, enlarged lymph nodes appear homogeneous and have been described as foamy in a p ~ e a r a n c eCalcification .~~ of cervical lymph nodes can be seen in sarcoidosis and appears to be related to the duration of disease." Swelling in the parotid region can result from enlargement of the parotid gland or lymphadenopathy within or adjacent to the parotid space (Fig. 7). Enlargement of the parotid gland in sarcoidosis is not usually accompanied by sialectasis. This distin-

SARCOIDOSIS

Sarcoidosis is a chronic multisystem noncaseating granulomatous disorder of uncertain cause. Although any organ system can be involved, the lungs, lymph nodes, skin, eyes, and salivary glands are most frequently affected.2yThe most common otolaryngologic manifestations are neck masses, parotid masses, and facial nerve palsy.33 Cervical

Figure 7. A 16-year-old girl with sarcoidosis and bilateral parotid enlargement. Axial FSEIR MR reveals bilateral homogeneous parotid enlargement (open arrows).

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guishes this condition from chronic parotid enlargement caused by chronic recurrent parotitis of childhood and Sjogren syndrome in which multiple small intraparotid cystic spaces are seen on CT and MR imaging.

SUMMARY

Cervical lymphadenopathy is the most common presentation of granulomatous inflammation of the neck in children and is usually caused by NTM infection. Although certain granulomatous infections have characteristic imaging features, there is considerable overlap in the imaging appearance of the various disorders. The diagnosis is usually based on a combination of clinical features, histopathologic examination, serologic tests, and culture results.

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IMAGING OF GRANULOMATOUS LESIONS OF THE NECK IN CHILDREN 37. Som I'M: Lymph nodes. In Som PM, Curtin HD (eds): Head and Neck Imaging, vol 2, ed 3. St. Louis, Mosby, 1996, pp 772-793 38. Spach DH, Koehler JE: Bartonella-associated infections. Infect Dis Clin North Am 12137-155, 1998 39. Spires JR, Smith RJ: Cat-scratch disease. Otolaryngol Head Neck Surg 94:622427, 1986 40. Stanley RB, Femandez JA, Peppard SB: Cervicofacial mycobacterial infections presenting as major salivary gland disease. Laryngoscope 93:1271-1275, 1983 41. Stewart MG, Starke JR, Coker NJ: Nontuberculous mycobacterial infections of the head and neck. Arch Otolaryngol Head Neck Surg 120:873-876, 1994 42. Taha AM, Davidson PT, Bailey WC: Surgical treatment of atypical mycobacterial lymphadenitis in children. Pediatr Infect Dis 43664-667, 1985 43. Thompson JN, Watanabe MJ, Greene GR, et al: Atypi-

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cal mycobacterial cervical adenitis: Clinical presentation. Laryngoscope 90:287-294, 1980 44. Tunkel DE, Romaneschi KB: Surgical treatment of cervicofacial nontuberculous mycobacterial adenitis in children. Laryngoscope 105:1024-1028, 1995 45. Umlas SL, Jaramillo D: Massive adenopathy in oropharyngeal tularemia: CT demonstration. Pediatr Radiol 20:483-484, 1990 46. Vazquez E, Enriquez G, Castellote A, et al: US, CT, and MR imaging of neck lesions in children. Radiographics 15:105-122, 1995 47. Wills PI, Gedosh EA, Nichols DR Head and neck manifestations of tularemia. Laryngoscope 9 2 7 7 s 773, 1982 48. Young LL, Dolan CT, Sheridan PJ, et al: Oral manifestations of histoplasmosis. Oral Surg Oral Med Oral Pathol 33:191-204, 1972 Address reprint requests to: Caroline D. Robson, MB, ChB Department of Radiology Children's Hospital 300 Longwood Avenue Boston, MA 02115