Chapter 248. Actinomycosis

Nahed Abdel-Haq; Ashir Kumar

Actinomycosis: Introduction

Actinomycosis is a slowly progressive suppurative infection characterized by fistula formation. A number of gram positive, non spore forming bacteria from the genus Actinomyces are the etiologic agents.1-3 It is encountered worldwide in three main clinical forms: cervicofacial, thoracic, and abdominal.1 Metastatic lesions to other sites are also reported. With appropriate therapy, most patients with cervicofacial or abdominal infection recover completely.

Etiologic Agent and Pathogenesis

Actinomyces species are part of the normal flora of the human gastrointestinal tract. They do not inhabit the female genitourinary tract in the absence of an intrauterine device (IUD).4 Actinomycosis is not considered an opportunistic or communicable disease. Although uncommon in children, actinomycosis has been reported in infancy.5 The disease is not related to occupation, season, or race.

A. israelii, the species that most commonly produces human disease, is part of normal oral flora. A. viscosus, A. naeslundii, A. odontolyticus, A. meyeri, and Propionibacterium (Arachnia) propionica are also established etiologic agents.1-3 Cervicofacial and abdominal infections are thought to occur when these organisms are traumatically introduced into tissues.6 Predisposing factors for actinomycosis include gingivitis, gingival trauma, dental procedures, tooth-related infections, diabetes mellitus, malnutrition, immunosuppression, and local tissue damage from different causes including trauma, radiation, and neoplasia as well as the use of an IUD.7,8 It has been shown than Actinomyces sp require the presence of other bacteria to multiply. Thus, actinomycosis is frequently polymicrobial in nature, and concomitant bacterial species such as Eikenella corrodens, Actinobacillus actinomycetemcomitans, Fusobacterium, Capnocytophaga, Staphylococcus, microaerophilic streptococci, and Enterobacteriaceae are often isolated from actinomycotic lesions.9-11Actinomyces sp require an anaerobic or microaerophilic environment for growth and demonstrate gram positive branching filaments, often appearing as beaded filaments.

A pivotal step in pathogenesis is the disruption of mucosal barriers, allowing access of these organisms to deep tissue. Thus, oral and cervicofacial disease are associated with dental procedures, trauma, and oral surgery.7 However, actinomycotic infections are infrequent, and some cases of actinomycosis may even develop after minor trauma such as eruption of a normal tooth.7 In fact, actinomycosis may not develop after major oral trauma or surgery. This indicates that oral or mucosal trauma alone is not the only factor responsible for actinomycotic infections. Other conditions may be required for Actinomyces sp to proliferate and establish an infection. These include the duration and severity of trauma that induce the microaerophilic environment as well as the synergistic effect of other bacteria.12 Abdominal infection is preceded by gastrointestinal surgery, appendicitis, diverticulitis, traumatic injury secondary to gunshot or knife wounds, or foreign bodies such as fish bones.11 Pelvic actinomycosis is associated with intrauterine devices.8 Pulmonary disease is believed to be secondary to aspiration.1 Once inoculated, the organism replicates and spreads contiguously in a slow and progressive manner with little respect for tissue planes. An acute inflammatory stage with a painful, cellulitic reaction is occasionally seen; however, most lesions progress to a chronic stage without significant early cellulitic reaction. The lesions present as masses with characteristic “wooden” walls due to extensive fibrosis. As the lesion matures it becomes soft and fluctuant, forming sinus tracts.1

Clinical Manifestations

Actinomycosis may present either as a chronic indolent process or as an acute rapidly progressive infection; the clinical manifestations may vary between these two extremes. However, the most common presentation remains the chronic indolent form.12

Cervicofacial Disease

Cervicofacial disease, accounting for 60% of patients with actinomycosis, presents as a slowly progressive, indurated swelling or mass, usually at the angle of the jaw, but it can occur anywhere on the cheek, mandible, or anterior neck.7 The duration of illness is typically several months. Pain is seldom prominent. A low grade fever may occur in as many as 50% of patients. Trismus is uncommon.13

The clinical progression may be marked by episodes of suppuration that are contained by reactive fibrosis. Although the lesions may be intermittently fluctuant and appear as a cold abscess, they will eventually progress to a hard mass with lumpy appearance.7 The disease spreads to adjacent tissues without regard to anatomical structures. Lymphatic spread and associated lymphadenopathy are uncommon.13 The skin overlying the mass may become violaceous, and sinus tract formation with spontaneous discharge often occurs. These sinus tracts have little tendency to heal and may remain chronic.14 There may be associated trismus. The drainage may reveal 1-mm diameter yellow friable masses termed sulfur granules, which are actually colonies of Actinomyces.14 Most patients do not appear systematically ill. The inflammatory markers such as the erythrocyte sedimentation rate and C-reactive protein as well as the white blood cell counts are often normal.13 The diagnosis of actinomycosis should be considered in virtually any chronic mass lesion or recurrent abscess in the head and neck region.

Maxillary and ethmoid sinusitis may occur.15 Actinomycosis is an uncommon but important cause of otitis media, as untreated cases can have fatal extension into the mastoid and central nervous system.16,17 As a cause of middle ear disease, actinomycosis is characterized by numerous episodes of otitis media that transiently respond to antibiotics (conventional short course therapy) and by resistance to myringotomy.16 Diagnosis can be made by microbiologic examination of material from the middle ear that appears to be a cholesteatoma.

Actinomycosis of the tonsils is rare and a poorly defined clinical entity. Actinomyces sp may be isolated from tonsillar crypts of both inflamed and uninflamed tonsils.61 Patients with tonsillar actinomycosis may present with coughing and expectoration of particulate material or a tonsillar mass.62Actinomyces sp may have a role in tonsillar hypertrophy. Patients with tonsillar actinomycosis may require tonsillectomy particularly if antibiotic treatment fails.62

Actinomycosis of the thyroid is another rare clinical entity. Predisposing factors include the persistence of a thyroglossal duct or a pyriform sinus fistula which facilitates the communication between the oral flora and the thyroid gland.68 Acute thyroiditis and abscess have been reported.5 An affected child may present with a painless neck mass.69 Treatment is a combination of surgical drainage and antibiotics.

Central nervous system involvement has been documented in 2% to 10% of cases of cervicofacial actinomycosis.17,18 Mechanisms of CNS infection include direct extension from soft tissues, orbit, sinus, or auditory canal, spread through foramina, and perineural spread.18 Most cases of CNS actinomycosis, however, are due to hematogenous or lymphatic spread from a distant focus such as the lungs, mouth, abdomen, and pelvis.19,20 Spread to the meninges may cause meningitis, meningoencephalitis, and brain abscess. Other forms of CNS involvement include tumor-like lesions called actinomycetomas as well as subdural and epidural abscesses.20

Cervicofacial actinomycosis presents as a chronic mass lesion or recurrent abscess in the head and neck region. Maxillary and ethmoid sinusitis may also occur.15 Another presentation is with recurrent episodes of otitis media that transiently respond to antibiotics (conventional short-course therapy) and by resistance to myringotomy.16 Fatal extension into the mastoid and central nervous system also occurs.16,17Central nervous system involvement has been documented in 2% to 10% of cases of cervicofacial actinomycosis, being due to either direct extension from soft tissues through the cranial foramen, or hematogenous spread.17-20 Spread to the meninges may cause meningitis, meningoencephalitis, and brain abscess. Other forms of CNS involvement include tumorlike lesions called actinomycetomas as well as subdural and epidural abscesses.20

Thoracic Disease

Thoracic involvement accounts for about 15% of patients with actinomycosis. It results from inhalation of contaminated aerosol particles or aspiration of contaminated secretions from the oropharynx or the upper gastrointestinal tract.21 However, it may also arise from a perforating gastrointestinal ulcer or after the intestinal mucosa is penetrated by a sharp object such as a knife, ingested bone, or bullet.11Abdominal actinomycosis may also follow gastric bypass surgery.30 Less commonly, pulmonary involvement occurs following esophageal perforation or as an extension of cervicofacial or abdominal disease.22 Poor oral hygiene is a predisposing condition. Immunocompromised patients are at increased risk.23 Thoracic actinomycosis is rare in children and young adults. Most cases are due to A. israelii.23 The most common presentation is a slowly progressive disease involving the parenchyma and pleura.24 As the disease progresses, the lung becomes consolidated and an abscess may form; the pleura and thoracic wall are invaded and produce empyema, rib involvement, subcutaneous abscesses, or draining sinuses.25 Hemoptysis has been reported.26 Delayed diagnosis may result in bacteremic dissemination with increased mortality rates.27 Pulmonary actinomycosis must be differentiated from nocardiosis, tuberculosis, fungal infections, and cancer. Mediastinal actinomycosis is uncommon. Due to the slow progression of the disease, if bone is involved, both destruction and new bone formation occur, producing wavy periostitis in the ribs or sawtooth changes in the vertebral bodies.22,23 Isolation of Actinomyces sp in sputum cultures is unusual.26 This is frequently due to the overgrowth of synergistic bacteria, prior use of antibiotics, and improper handling of anaerobic cultures. In addition, Actinomyces sp are found normally in saliva samples. Transbronchial biopsy or needle aspiration biopsy may be used to confirm the diagnosis. However, surgery is frequently needed to establish the diagnosis.28 Other indications for surgery are recurrent or severe hemoptysis, prolonged illness, poor response to antibiotics, and suspected carcinoma.26

Cardiac actinomycosis is rare and follows direct spread from pulmonary disease. Pericardial involvement is the most common form.63 Myocarditis and endocarditis are less frequent.64,65 The clinical presentation of pericarditis is more insidious than other causes of purulent pericarditis. The yield of pericardial cultures is low. The diagnosis is usually made by histopathologic identification of the typical Actinomyces filaments and sulfur granules in pericardial biopsy.64 Esophageal actinomycosis is a rare clinical entity that mainly affects immunocompromised patients including those with cancer or HIV infection.66,67 Dysphagia and odynophagia are the most frequent complaints. Esophageal ulceration is usually seen during esophagoscopy. Diagnosis is made by histopathology of biopsy samples; the yield of culture is low.66

Abdominal Disease

Abdominal actinomycosis accounts for 20% of patients.1 Any organs and anatomical structures in the abdomen may be involved. The majority of cases begin in the ileocecal region as a complication of appendicitis or appendectomy (65% of cases).29However, it may also arise from a perforating gastrointestinal ulcer or after the intestinal mucosa is penetrated by a sharp object such as a knife, ingested bone, or bullet.11 Abdominal actinomycosis may also follow gastric bypass surgery.30 Abdominal infections are polymicrobial; gram-negative bacilli are frequent concomitant pathogens.11 The initial symptoms are insidious and include abdominal discomfort, fever, weight loss, change in bowel habits, and malaise. Abdominal tenderness and guarding in the right iliac fossa are common with perforated appendix.31 Months to years may pass from the time of the inciting event to clinical recognition of this indolent infection. During the initial stage of infection, an abscess forms that is followed by extension to the peritoneum. The abscess consists of pus surrounded by a thick layer of granulation tissue. Abdominal examination often reveals a mass. In advanced stages, the disease progresses to fistula formation, both internally and externally, simulating inflammatory bowel disease.32 Abscess rupture through the abdominal wall produces a typical draining sinus from which sulfur granules are detected.32 Colonic involvement accounts for approximately 15% of abdominal actinomycosis, presenting with obstruction or fistula.35 Hepatic infection occurs in 5% of cases of abdominal actinomycosis, usually by direct extension. Most cases are unilobar.42 Isolation of Actinomyces sp or identification of characteristic sulfur granules in sinus drainage material is diagnostic. However, in the absence of these findings, differentiation from appendicitis, regional enteritis, cancer, abscess, tuberculosis, amebiasis, and other intra abdominal disorders may only be possible after a biopsy.11,29 The infection may extend to involve the liver, other abdominal organs, and spine, or it may penetrate the diaphragm to produce thoracic disease.33,34

Colonic involvement accounts for approximately 15% of abdominal actinomycosis.35 Most cases occur in the left colon or caecum in association with IUD-related pelvic disease.36,37 Patients may present with symptoms and signs of left colonic obstruction.38 Primary perianal and perirectal disease is rare. However, perianal lesions may result from extension of pelvic infection or abdominal disease.39 A recurrent fistula that fails to heal after drainage or fistulotomy is suggestive of actinomycosis.40 These lesions occur more commonly in immunocompromised patients.41

Hepatic infection occurs in 5% of cases of abdominal actinomycosis, usually by direct extension. Most cases are unilobar.42 Patients present with nonspecific signs and symptoms.43 The ultrasound may show an abscess or a solid mass suggestive of a tumor. Most hepatic abscesses can be drained percutaneously in contrast to abscesses elsewhere in the abdomen. Rarely, actinomycosis may present secondary to hematogenous spread to the liver. Biliary actinomycosis may be indistinguishable from other bacterial causes.44 Involvement of the stomach, small intestine, and pancreas is unusual. Gastric actinomycosis may follow peptic ulcer or bariatric surgery.45 A palpable epigastric mass is common. The clinical manifestations of gastric actinomycosis are similar to carcinoma; however, fever and leukocytosis are often present.46

Renal involvement is also rare and often occurs due to direct extension from pelvic or abdominal abscesses.47 Hematogenous seeding of the kidney may rarely occur. Most cases of renal actinomycosis are diagnosed following nephrectomy for renal masses. However, nephrectomy can be avoided by suspecting the diagnosis and obtaining fine needle aspirate and biopsy.48,49

Pelvic Disease

Pelvic actinomycosis is commonly associated with the presence of any type of intrauterine contraceptive device (IUD) and appears to occur rarely unless the IUD has been in place for at least 2 years.50 It has been reported months after removal of an IUD, making a history of prior use important.51Actinomyces sp have been identified in 8% to 20% of women using IUD. Although most of those colonized individuals are asymptomatic, up to 25% developed symptoms of pelvic infection.52,53 Presentation is most frequently that of an indolent infection, with fever, weight loss, abnormal vaginal bleeding, and pain being common. A “frozen pelvis,” due to the fibrosis, mimicking malignancy may develop.54 Less frequently, patients may present more acutely if the concomitant pathogen is Staphylococcus aureus or beta-hemolytic streptococci. Pelvic actinomycosis may be associated with nonspecific clinical and laboratory findings such as fever with elevated white blood cells and C-reactive protein. Actinomycosis should be considered in women using IUD who present with any abdominal pathology.55 Tubo ovarian abscess is an early presentation.56 Involvement of the bladder and ureters may cause hydroureter and hydronephrosis. Extensive disease leading to liver abscesses and pleural effusion has also been reported.34,55 Women frequently undergo surgery because of suspicion of ovarian cancer because of masses due to pelvic actinomycosis.54 Pelvic actinomycosis may develop into firm indurated fibrotic masses that may be associated with increased incidence of complications in adjacent organs such as ureteral and bowel obstruction.59,60 Because of the extensive soft tissue involvement and the lack of well-defined surgical margins, early surgical intervention in stable patients is limited to relief of obstructive symptoms or to drain large abscesses.8 Surgery is, however, indicated in patients with no clinical or radiological evidence of improvement on antibiotic treatment.8

Other Disease Sites

Rarely, actinomycotic skin and soft tissue lesions mimicking tumors are seen in extremities, possibly secondary to traumatic inoculation.70 Human bites have caused localized skin infections with Actinomyces species.71

Diagnosis

The diagnosis of actinomycosis is obvious when a draining sinus in the neck, chest, or abdomen produces sulfur granules.14,32 The presence of Actinomyces-like organisms on Papanicolaou-stained cervical specimens associated with pain, abnormal bleeding, or discharge, is an indication for removal of an IUD and a 14-day course of penicillin or tetracycline.56 However, the presence of Actinomyces sp on cervical smear in an asymptomatic woman does not require IUD removal or antibiotic therapy.58

Imaging studies such as computed tomography and magnetic resonance imaging will show the actinomycosis lesions as ill-defined, infiltrative, soft tissue masses extending to surrounding spaces without regard to anatomic facial planes.36 Regional lymphadenopathy is uncommon; this finding may be helpful to differentiate actinomycosis from carcinoma.6 The diagnosis of pelvic actinomycosis can be established on clinical grounds or following microbiological identification from material obtained by needle aspiration or surgical drainage. The Actinomyces sp may also be demonstrated in cervical smears and endometrial biopsies.57 Such granules may be seen normally in the tonsil.61Microscopic examination of these granules reveals gram positive beaded filaments that are not acid fast. The bacteriologic identification from sulfur granules or a sterile site confirms the diagnosis. However, sulfur granules are not always present and biopsies for culture and histopathologic evaluation are frequently needed for diagnosis of actinomycosis in different tissues.11,29 Pathologic examination of a biopsied lesion will reveal a central suppurative area surrounded by chronic granulation tissue, and a thick fibrous capsule. In biopsy samples, the sulfur granules, if present, are found in the necrotic centers and are characteristic but not pathognomonic of actinomycosis. They can be produced by other bacteria such as Staphylococcus aureus, Nocardia, and Actinobacillus lignieresii, and fungi such as Sporotrichum and Phialophore14,72; although typically these organisms lack the peripheral clubs seen in Actinomyces species. Grossly, they are hard and gritty. They appear round or oval in shape. They may be yellow, white, pinkish gray, gray, or brown in color. Histologically, the sulfur granules are masses of filaments extending in a radiating appearance. The filamentous mass is hardened and mineralized by calcium phosphate deposits due to phosphatase enzyme activation by tissue inflammation. Club-like extensions at the end of the filaments are due to aggregation of inflammatory cells, mainly neutrophils, and deposition of polysaccharide–protein matrix.14 Coccoid forms of the bacteria will be found among these filaments. With hematoxylin and eosin stain, the central core will be basophilic, and the peripheral clubs will be eosinophilic. Special fungal stains are negative. Older filamentous structures may stain with methenamine silver stain.73 The surrounding granulation tissues consist of inflammatory cells mainly lymphocytes, plasma cells, epithelioid cells, and histiocytes and occasional giant cells.73 The outermost layer is the capsule that is characteristically intensely collagenous, fibrotic, and avascular.9 The capsule helps maintain the anaerobic environment, limits antibiotic penetration, and allows for the progression of infection.

Actinomyces sp are easily grown below the surface in thioglycollate medium, provided the inoculum does not contain other organisms. Growth usually appears within 5 to 7 days but may take up to 2 to 4 weeks.14 Because these organisms are normal flora of the oral cavity and female genital tract, isolation of the organisms is not sufficient for diagnosis in the absence of sulfur granules. In addition to culture, the use of immunofluorescent-conjugated monoclonal antibodies (IFAs) has improved identification of Actinomyces species. Use of IFA allows species identification in fixed tissue or sulfur granules directly.1 Serology is not reliable and not useful for diagnosis. Cross-reaction has been reported with tuberculosis.14 Rapid diagnostic tests to detect specific antibodies to Actinomyces sp are under development.74

Treatment

Prolonged and intensive penicillin therapy and surgery remain the mainstay of treatment of most cases of actinomycocsis.1 Penicillin is the drug of choice for treatment. Initially, intravenous aqueous penicillin, 200,000 U/kg per day (maximum dose: 18–24 million units/d) should be given for 2 to 4 weeks for cervicofacial disease and 4 to 6 weeks for pulmonary and abdominal infection, depending on the extent of the disease and response to therapy. Subsequently, patients should receive oral penicillin V , for 6 to 12 months. Patients allergic to penicillin may be treated with erythromycin, clindamycin, chloramphenicol, or tetracycline (minocycline).77 Oral amoxicillin is probably of equal efficacy.75 If the duration of treatment is not extended beyond the resolution of measurable disease, relapses will occur. Successful treatment with short-term courses of antibiotics (< 6 months) has been reported.76 Patients who responded to short courses typically had localized disease and underwent appropriate drainage procedures. The decision to treat with short courses should be individualized and based on the extent of the disease and response to treatment.5,69,76 Isolates of A actinomycetemcomitans are often resistant to penicillin. Antibiotics considered ineffective in treating actinomycosis include oxacillin, dicloxacillin, cephalexin, fluoroquinolones, aztreonam, and aminoglycosides.14,78 Accessible abscesses should be incised and drained. Because extensive fibrosis may limit antibiotic penetration of the abscess, surgical excision should be considered for refractory fibrotic lesions that respond slowly to antibiotic therapy. Persistent sinus tracts should be marsupialized. Surgical management should always be accompanied by effective antibiotic therapy.11,55

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