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AJR 2001; 176:341-349
© American Roentgen Ray Society

Review

Imaging Characteristics and Epidemiologic Features of Atypical Mycobacterial Infections Involving the Musculoskeletal System

Daphne J. Theodorou1,2, Stavroula J. Theodorou1,2, Yousuke Kakitsubata1,2, David J. Sartoris1,3,4 and Donald Resnick1,2

1 Department of Radiology, School of Medicine, University of California, San Diego Medical Center, San Diego, CA 92103.
2 Department of Radiology, Veterans Affairs Medical Center, 3350 La Jolla Village Dr., San Diego, CA 92161.
3 Department of Radiology, UCSD Medical Center, Thornton Hospital, 9300 Campus Point Dr., La Jolla, San Diego, CA 92037-7756.
4 Deceased.

Received June 7, 1999; accepted after revision June 1, 2000.

 
Supported by VA grant SA-360 and the A. S. Onassis Public Benefit Foundation grant U-033.

Address correspondence to D. Resnick.


Introduction
Top
 Introduction
Epidemiologic Features
 Clinical Aspects
 Osteoarticular Manifestations
 Soft-Tissue Manifestations
 Conclusion
 References
 
Although radiologists are interpreting images of immunocompromised patients who have atypical mycobacterial infections more often, radiologists may not be familiar with the musculoskeletal manifestations of atypical mycobacterial disease. We review the imaging features of atypical mycobacterial infections involving the musculoskeletal system, illustrate a wide range of these abnormalities, and present the epidemiologic characteristics of atypical mycobacterial strains known to be associated with disease in humans.


Epidemiologic Features
Top
 Introduction
 Epidemiologic Features
Clinical Aspects
 Osteoarticular Manifestations
 Soft-Tissue Manifestations
 Conclusion
 References
 
"Atypical" mycobacteria are mycobacterial isolates that have colonial characteristics that are different from Mycobacterium tuberculosis. Although these bacteria were initially regarded as saprophytes, it was not until the 1950s that atypical mycobacteria were recognized as human pathogens. Because there is no evidence of human-to-human transmission of atypical mycobacteria, they do not pose public health hazards [1,2,3], and unlike M. tuberculosis, atypical mycobacteria are usually drug-resistant organisms [4].

As the incidence of tuberculosis in the United States has declined, the absolute and the relative (to tuberculosis) incidence of atypical mycobacterial infections have increased [2, 5]. This increased incidence is not a result of the impact of HIV infection because the increase occurred before the appearance of AIDS [5]. This increase possibly relates to the increased awareness of health care providers as well as the increased virulence of atypical mycobacteria [6]. Atypical mycobacterial infections account for 0.5-30% of all mycobacterial infections [7]. In the most recent survey performed by the Centers for Disease Control and Prevention, atypical mycobacteria were found to account for 35% of isolations (not cases) of pathogenic mycobacteria [8]. National surveys conducted in the United States by the Centers for Disease Control and Prevention during the years 1981-1983 showed the incidence of atypical mycobacterial infections to be 1.78 cases per 100,000 population [9].

Although humans are routinely exposed to atypical mycobacteria, the rate of clinical infection is low because the bacteria usually colonize rather than invade the host [3]. Depending on the specific strain and host, however, these bacteria can cause various infections; such infections usually occur in the elderly [7] and in patients who are immunocompromised [1, 10,11,12,13].

Involvement of the musculoskeletal system occurs in approximately 5-10% of patients with atypical mycobacterial infections [14]. Musculoskeletal infection is acquired by contamination from surgical procedures or penetrating injuries and hematogenous spread [1, 11]. In particular, atypical mycobacterial strains usually acquired by trauma are Mycobacterium fortuitum, Mycobacterium chelonae, and Mycobacterium marinum [15].

Atypical mycobacteria have been isolated from soil, water, milk, birds, fish, and animals [16]. Although atypical mycobacterial are ubiquitous in nature, they have a variable geographic distribution [17,18,19,20]. The strains of atypical mycobacteria associated with human disease with reference to musculoskeletal system involvement and specific reservoir for each strain are listed in Table 1.


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  		TABLE 1 Atypical Mycobacteria Known to Cause Musculoskeletal System Infections in Humans and Reservoir of These Mycobacteria

 

In contradiction to tuberculosis, atypical mycobacterial infections are not reported in most areas [2]. A general observation is that in the United States atypical mycobacteria are found mainly in the South [21]; epidemiologic studies from different parts of the world, however, indicate that different species predominate as a cause of disease in different geographic areas.


Clinical Aspects
Top
 Introduction
 Epidemiologic Features
 Clinical Aspects
Osteoarticular Manifestations
 Soft-Tissue Manifestations
 Conclusion
 References
 
Clinically, musculoskeletal infections caused by atypical mycobacteria resemble those caused by M. tuberculosis [1, 10, 22], although the overall course of atypical mycobacterial disease is often milder than that of tuberculous infection [10]. In children, however, atypical mycobacterial disease can be more aggressive and can result in growth disturbance [23].

With atypical mycobacterial infection, onset of nonspecific symptoms is indolent and usually includes local pain and swelling, joint stiffness, low-grade fever, sweats, chills, anorexia, malaise, and weight loss. With the dissemination of infection, diffuse involvement of the reticuloendothelial system, including bone marrow [24], is seen, and osseous manifestations are common. On histopathologic examination, a spectrum of inflammatory changes have been reported [24,25,26,27] including granulomatous lesions with or without caseation.

The clinical course of disease is typically protracted [7], and the average time to diagnosis from the onset of symptoms may be up to 10 months [28,29,30]. Accurate diagnosis and effective treatment of an atypical mycobacterial infection of the musculoskeletal system are mandatory to prevent severe bone and joint destruction and possible neurologic complications in cases of spinal involvement. In this respect, tissue sampling and culturing may validate diagnosis. In the setting of cultures with negative findings, however, DNA amplification and subsequent determination of the nucleic acid sequence have reportedly been helpful in identifying the pathogen [31].

Prescribed medications in the setting of atypical mycobacterial infection are the combination of different antituberculous drugs and antibiotics to which the isolates are sensitive [32]. Just as in patients with tuberculosis, the outcome of treatment in patients with mycobacterial infections is more favorable in previously healthy individuals than in patients with underlying disease [32, 33]. Because antimycobacterial chemotherapy alone usually is not sufficient in improving musculoskeletal manifestations, surgical treatment may be needed [25, 34, 35].


Osteoarticular Manifestations
Top
 Introduction
 Epidemiologic Features
 Clinical Aspects
 Osteoarticular Manifestations
Soft-Tissue Manifestations
 Conclusion
 References
 
As with other infectious agents that cause osteomyelitis, atypical mycobacteria can contaminate bone by two principal routes: hematogenous spread of infection (Fig. 1A,1B) and direct introduction of pathogens from environmental or contiguous sources, such as an infection in the adjacent soft tissues or joints [23]. Most osseous infections, however, are caused by Mycobacterium kansasii and Mycobacterium scrofulaceum followed in frequency by Mycobacterium avium-intracellulare and M. fortuitum [10].



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  		Fig. 1A. —5-year-old emaciated girl, weighing only 10 kg, who presented with remarkable bone pain and inability to walk. Patient had cystic pattern of mycobacterial osteomyelitis. Histopathology (not shown) of lesions yielded Mycobacterium kansasii. Frontal radiograph shows extensive destructive areas (arrows) in skull involving frontal, temporal, and parietal regions. Greater wing of sphenoid bone on left side cannot be seen.

 


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  		Fig. 1B. —5-year-old emaciated girl, weighing only 10 kg, who presented with remarkable bone pain and inability to walk. Patient had cystic pattern of mycobacterial osteomyelitis. Histopathology (not shown) of lesions yielded Mycobacterium kansasii. Frontal radiograph shows gross destruction of right ischium (straight arrow), soft-tissue swelling, and lytic involvement of right proximal femur (curved arrow). Note extensive, reactive osseous sclerosis and periosteal new bone formation (arrowheads).

 

Osteomyelitis caused by atypical mycobacteria resembles acute pyogenic infection but is characterized by slower progression [33]. Early radiographic findings may consist of subtle soft-tissue swelling related to inflammatory changes and regional hyperemia, the latter resulting in bone resorption within a few days after implantation of mycobacteria into the bone. As the infection progresses, further osteolysis, cortical resorption, and medullary edema ensue. In patients with acute osteomyelitis caused by atypical mycobacteria, it may take several weeks for the osteolysis and periostitis to become evident radiographically. In patients with subacute and chronic osteomyelitis, bone abscesses, sequestrum formation, osseous deformity, mature periosteal reaction and involucrum formation (a zone of living bone surrounding sequestered bone), and sinus tracts are characteristic radiographic findings [23]. Given the delay in diagnosis [28,29,30, 36], most cases of atypical mycobacterial infection are recognized during the subacute stage of osteomyelitis [22, 37,38,39].

Overall, although radiographic features for each strain of atypical mycobacteria involving the musculoskeletal system have not been well defined, general observations include the following traits: preferential involvement of the metaphyses and diaphyses of long bones, multiple sites of involvement, and discrete lytic areas with marginal sclerosis and osteoporosis that may not be as striking as in cases of tuberculosis [11].

Because similar findings may be encountered in tuberculous osteomyelitis, differentiation between tuberculous and atypical mycobacterial infection on the basis of radiographic features is not feasible in most cases. With tuberculous infection, the following three radiologic patterns of bone involvement are typically described [11, 40]: tuberculous dactylitis (spina ventosa), which is an expanding destructive lesion of both cortical and cancellous bone with periostitis; honeycombing, which is a diffuse uniform lesion with cavitation and relatively little osteoporosis; and cystic tuberculosis, which presents as multifocal, well-defined, round or oval radiolucent lesions, often with a sequestrum accompanied by osteoporosis and variable amounts of sclerosis (Fig. 1A,1B). Bone-marrow biopsy usually allows diagnosis of atypical mycobacterial infection and the identification of the causative mycobacterium isolate.

In the spine, atypical mycobacterial osteomyelitis shares similar morphologic abnormalities with tuberculous spondylitis (Pott's disease) [10]. Diagnostic criteria for mycobacterial osteomyelitis affecting the spine may include the following: involvement of one or several contiguous vertebral bodies that may result in kyphosis; destruction of the intervening disks; absence of reactive sclerosis; and formation of soft-tissue abscesses, usually containing calcification, that may be vertebral or extradural or that may spread into adjacent structures including the buttocks, abdominal wall, and thigh [11, 41,42,43] (Fig. 2A,2B,2C). Additional features of spine infection may include involvement of only a single end plate and involvement of noncontiguous levels. In patients with mycobacterial spondylitis, local tenderness, pain, and limitation of spinal mobility are the presenting symptoms, whereas constitutional symptoms such as fever, malaise, and weight loss may also occur. On neurologic examination, evidence of compressive neuropathy with or without paralysis may be revealed.



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  		Fig. 2A. —41-year-old man who presented with low back pain resulting from vertebral osteomyelitis caused by Mycobacterium kansasii. Lateral radiograph of lower lumbar spine shows extensive destruction of fourth lumbar vertebral body (open arrow) and marked narrowing of intervertebral disk space (solid arrow). Upper end plate of fifth lumbar vertebra appears unremarkable. With this type of infection, involvement of only one vertebral end plate, as in this patient, is not rare.

 


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  		Fig. 2B. —41-year-old man who presented with low back pain resulting from vertebral osteomyelitis caused by Mycobacterium kansasii. Unenhanced contiguous T1-weighted spin-echo MR images (TR/TE, 630/25) show intermediate signal intensity in lower part of fourth lumbar vertebral body and adjacent intervertebral disk (arrow). Area of severe bone destruction is delineated by margin of low signal intensity (arrowheads), which represents reactive sclerosis.

 


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  		Fig. 2C. —41-year-old man who presented with low back pain resulting from vertebral osteomyelitis caused by Mycobacterium kansasii. Corresponding T2-weighted spin-echo MR images (2000/80) show abnormal high signal intensity of fourth lumbar vertebral body (curved arrow) and intervening disk (straight arrow). Note that fifth lumbar vertebra is spared.

 

Radiography is well suited for revealing the most important hallmarks of osteomyelitis, which include permeative osteolysis, bone sequestration, and periostitis. However, early radiographic findings of osteomyelitis may be inconspicuous; in addition, the radiographic features of acute osteomyelitis can resemble those associated with malignant bone tumors, pyogenic or fungal infections, neuropathic osteoarthropathy, reflex sympathetic dystrophy, transient regional osteoporosis, stress fractures, and healing fractures [11, 23].

In ambiguous cases of mycobacterial osteomyelitis, cross-sectional imaging techniques prove useful. CT is of great value in depicting early erosion in cortical bone, bone fragmentation, small accumulations of fluid, and cloacae (openings in the involucrum) [10, 23]. Unlike radiography, CT can adequately depict early infection, which is revealed as increased intraosseous density that corresponds to the accumulation of pus replacing bone marrow fat. In addition, CT may be helpful in evaluating bone sequestra, which appear as fragments of necrotic bone separated from living bone by soft tissue or fluid density, and in guiding percutaneous biopsy of infected areas [44, 45]. Furthermore, contrast-enhanced CT may also facilitate visualization of abscesses and necrotic tissue. In the clinical setting of mycobacterial spondylitis, CT in conjunction with MR imaging may provide supplemental diagnostic information regarding paraspinal and intraspinal extension of infection and may characterize the extent of bone and disk involvement [11, 44, 46], which may escape detection on conventional radiography. Furthermore, cross-sectional imaging may aid in limiting the differential diagnosis of mycobacterial spondylitis, which includes pyogenic or fungal infections, primary and metastatic tumors of the spine, and sarcoidosis [10, 11, 45].

MR imaging is regarded as the most sensitive imaging method for the early detection of osteomyelitis. In patients with osteomyelitis, infected areas are displayed as regions of decreased signal intensity on T1-weighted sequences and of increased signal intensity on T2-weighted and short inversion time inversion-recovery sequences [45, 47,48,49,50,51,52,53,54,55,56]. This appearance results from replacement of marrow fat by inflammatory cells and exudate due to associated hyperemia [50]. Although MR imaging is not as helpful as CT in the evaluation of cortical erosion and disruption, MR imaging allows the display of the periosteal reaction. Enhanced fat-suppressed MR images, however, may provide better delineation of associated cellulitis, abscesses, and sinus tracts and may allow distinction between sequestered and living bone [57]. In spinal osteomyelitis, however, IV administration of a gadolinium-based contrast medium may allow detection and delineation of the extent of epidural involvement [44]. In this regard, MR imaging may indicate whether infection is limited to soft tissues or to bones and joints and may show the absolute extent of the inflammatory process, thus contributing to preoperative planning. Furthermore, given the capability of bone scanning to assess blood perfusion and osteoblastic activity, MR imaging in conjunction with radionuclide bone scanning may be useful in differentiating osteomyelitis from adjacent cellulitis [47, 50, 58].

Because other disorders including tumors, bone infarction, metabolic diseases, fractures, and surgical changes can present signal intensity characteristics similar to those associated with osteomyelitis [23, 52, 59], it is well accepted that MR imaging is of limited specificity in the diagnosis of osteomyelitis. However, an attribute of MR imaging in the clinical setting of suspected osteomyelitis, particularly during the acute phase of disease, is its high negative predictive value, which may eventually lead to an exclusionary diagnosis of disease. In patients with inconclusive clinical and MR imaging findings, aspiration or tissue sampling may be pursued to establish diagnosis.

Because atypical mycobacterial articular disease bears similar clinical and radiologic features with tuberculous articular disease [10, 22], it is imperative that joint involvement by atypical mycobacteria be considered during the diagnostic workup of monoarticular disease [10, 35, 60]. Just as in tuberculous arthritis, articular lesions occur as a result of adjacent osteomyelitis or, less commonly, as a sequela of primary synovial inflammation and may result in destructive arthritis [10, 11, 29, 61].

Early in the disease process, minimal inflammation that may include joint effusion and associated soft-tissue swelling in an otherwise normal joint may escape detection. Clinical history classically discloses an insidious onset of joint pain and swelling. Other presenting symptoms may include muscle wasting, weakness, joint stiffness, and draining sinuses. Radiographically, infectious invasion of the synovium is manifested initially as regional osteopenia, which characteristically is neither as extensive nor as severe as in tuberculous arthritis [11, 23]. As the disease progresses, marginal and subchondral osseous erosions are the dominant radiographic features. In children, chronic inflammatory synovitis and overgrowth of the epiphyses may result in premature physeal closure with subsequent leg-length discrepancy [62]. The findings of soft-tissue swelling, osteopenia, and marginal osseous erosions are, however, nonspecific [63] for atypical mycobacterial infection because these findings are also evident in other infectious diseases and in rheumatoid arthritis. In cases of mycobacterial inflammatory processes of joints, various degrees of cartilage destruction take place; however, destruction of the articular cartilage typically progresses slowly owing to the absence of proteolytic enzymes in the coexistent exudate [64]. In this regard, relative preservation of joint space until late in the disease is highly suggestive of mycobacterial arthritis, whereas early loss of articular space is more typical of rheumatoid arthritis [11]. The triad of Phemister, consisting of osteoporosis, peripheral marginal erosions, and slowly progressing destruction of articular cartilage, characterizes mycobacterial arthritis (Figs. 3A,3B,3C,3D,3E,4,5A,5B,5C,6,7A,7B,7C,7D). Less frequently, a linear pattern of periosteal reaction and bone proliferation may be seen. If untreated, mycobacterial arthritis can result in severe osseous destruction and fibrous ankylosis.



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  		Fig. 3A. —59-year-old man with history of sarcoid treated with steroids developed severe knee pain from septic arthritis that was caused by Mycobacterium avium-intracellulare. Constellation of findings including central and marginal lesions, diffuse and profound involvement of bone marrow, and absence of osteophytes militates against diagnosis of degenerative joint disease. (Courtesy of Beaulieu C, Stanford, CA) Unenhanced T1-weighted spin-echo MR image (TR/TE, 600/22) shows multiple areas of abnormally low signal intensity in both femoral and tibial condyles (solid arrows). Note peripheral joint erosions of femoral condyles (open arrows).

 


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  		Fig. 3B. —59-year-old man with history of sarcoid treated with steroids developed severe knee pain from septic arthritis that was caused by Mycobacterium avium-intracellulare. Constellation of findings including central and marginal lesions, diffuse and profound involvement of bone marrow, and absence of osteophytes militates against diagnosis of degenerative joint disease. (Courtesy of Beaulieu C, Stanford, CA) Corresponding fat-suppressed intermediate-weighted fast spin-echo MR image (3000/21) shows abnormal high-signal-intensity areas (curved arrows) delineating extent of marrow involvement. Note marginal erosions of femoral condyles (open arrows) and joint effusion. Adjacent soft tissues (arrowheads) appear edematous.

 


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  		Fig. 3C. —59-year-old man with history of sarcoid treated with steroids developed severe knee pain from septic arthritis that was caused by Mycobacterium avium-intracellulare. Constellation of findings including central and marginal lesions, diffuse and profound involvement of bone marrow, and absence of osteophytes militates against diagnosis of degenerative joint disease. (Courtesy of Beaulieu C, Stanford, CA) T2-weighted fast spin-echo MR image (2700/76) depicts high-signal-intensity foci surrounded by low-signal-intensity rim (arrows).

 


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  		Fig. 3D. —59-year-old man with history of sarcoid treated with steroids developed severe knee pain from septic arthritis that was caused by Mycobacterium avium-intracellulare. Constellation of findings including central and marginal lesions, diffuse and profound involvement of bone marrow, and absence of osteophytes militates against diagnosis of degenerative joint disease. (Courtesy of Beaulieu C, Stanford, CA) T2-weighted fat-suppressed spin-echo MR image (2117/80) shows abnormal signal intensity in femoral condyles and in tibial plateau (arrows). Joint effusion (e) and soft-tissue swelling (T) are also present.

 


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  		Fig. 3E. —59-year-old man with history of sarcoid treated with steroids developed severe knee pain from septic arthritis that was caused by Mycobacterium avium-intracellulare. Constellation of findings including central and marginal lesions, diffuse and profound involvement of bone marrow, and absence of osteophytes militates against diagnosis of degenerative joint disease. (Courtesy of Beaulieu C, Stanford, CA) Intermediate-weighted fast spin-echo MR image (2117/30) shows diffusely abnormal signal intensity of bone marrow (arrowheads), which is related to osteomyelitis. Note areas of low signal intensity in subchondral bone of femoral and tibial condyles. Joint effusion (e) is also present.

 


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  		Fig. 4. —65-year-old woman with history of puncture wound of distal phalanx from contact with fish spines who presented with swelling and pain at site of minor injury. Mycobacterium marinum was recovered from synovial biopsy. Frontal radiograph of digit shows soft-tissue swelling (arrowheads), marginal osseous erosion at corner of distal interphalangeal joint (curved arrow), and remarkable joint-space narrowing (straight arrows), consistent with septic arthritis and osteomyelitis.

 


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  		Fig. 5A. —37-year-old man who presented with long history of continuous pain and repeated effusions in knee joint from septic arthritis caused by Mycobacterium avium-intracellulare. Lateral radiograph shows large effusion (E) in knee joint. Osteopenia can also be seen. Cortical erosions of posterior aspect of medial femoral condyle and anterior aspect of lateral femoral condyle (solid arrows) are present. Narrowing of patellofemoral space and formation of patellar osteophytes (open arrow) are also revealed.

 


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  		Fig. 5B. —37-year-old man who presented with long history of continuous pain and repeated effusions in knee joint from septic arthritis caused by Mycobacterium avium-intracellulare. Unenhanced T1-weighted spin-echo MR image (TR/TE, 886/15) depicts patchy pattern of abnormal low signal intensity in medial femoral condyle (straight arrows), consistent with osteomyelitis. Posteromedial corner of tibia (curved arrow) is affected to lesser extent. Large joint effusion (e) and synovial cyst (c) are also present.

 


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  		Fig. 5C. —37-year-old man who presented with long history of continuous pain and repeated effusions in knee joint from septic arthritis caused by Mycobacterium avium-intracellulare. Enhanced fat-suppressed T1-weighted spin-echo MR image (700/20) shows effusion of joint and inhomogeneously low signal intensity within suprapatellar bursa caused by intraarticular infectious debris (thin arrow). Synovial cyst (C) also is evident. Note patchy, inhomogeneous enhancement of femoral condyles (arrowheads). Adjacent soft tissues (open arrows) appear edematous; soft-tissue defect (thick arrow) is also observed.

 


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  		Fig. 6. —29-year-old man who presented with 2-year history of left wrist pain, which reportedly began initially after trauma, that was caused by septic arthritis resulting from Mycobacterium avium-intracellulare. Frontal radiograph of wrist shows areas of lytic erosion involving distal ulna and radius, and the scaphoid, triquetrum, and pisiform bones (straight arrows). Moderate osteoporosis of radial styloid and of ulnar styloid processes (curved arrows) is also noted. Joint spaces are preserved. (Courtesy of Scavulli J, San Diego, CA)

 


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  		Fig. 7A. —2-year-old boy with septic arthritis of knee and osteomyelitis in proximal right tibia caused by Mycobacterium kansasii. (Courtesy of Yang BY, Kaoshiung, Taiwan) Anteroposterior radiograph of right tibia shows large multiloculated region of osteolysis involving epiphyseal, metaphyseal, and proximal diaphyseal area (curved arrow). Surrounding sclerosis (open arrow) and expansion of proximal tibia can be seen. Note fracture and fragmentation of tibial physis (straight arrow).

 


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  		Fig. 7B. —2-year-old boy with septic arthritis of knee and osteomyelitis in proximal right tibia caused by Mycobacterium kansasii. (Courtesy of Yang BY, Kaoshiung, Taiwan) Lateral radiograph of tibia shows lytic lesion (curved arrow) of medullary and cortical areas of proximal tibia. Bone expansion, reactive sclerosis (open arrow), and periostitis (straight arrow) can also be seen.

 


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  		Fig. 7C. —2-year-old boy with septic arthritis of knee and osteomyelitis in proximal right tibia caused by Mycobacterium kansasii. (Courtesy of Yang BY, Kaoshiung, Taiwan) Unenhanced CT image exhibits extensive cortical and medullary osteolysis (arrow) in unfused tibial epiphysis (E).

 


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  		Fig. 7D. —2-year-old boy with septic arthritis of knee and osteomyelitis in proximal right tibia caused by Mycobacterium kansasii. (Courtesy of Yang BY, Kaoshiung, Taiwan) Unenhanced CT image of tibial diaphysis (D) shows cortical and medullary osteolysis (straight arrow). Fracture with swelling of surrounding soft tissues (solid arrow), which is related to spread of infection, is also present.

 

In the diagnostic workup of mycobacterial arthritis, radiography commonly reveals a constellation of nonspecific findings, including soft-tissue swelling and regional osteopenia. Although it is generally accepted that the role of sonography in the detection of intraarticular abnormalities is limited, sonography may aid considerably in the documentation of joint effusion and synovial thickening [65]. Furthermore, sonography may also be useful in guiding diagnostic aspiration and therapeutic drainage of intraarticular fluid collections [65].

Because early diagnosis of joint infection is important, cross-sectional imaging (Figs. 3A,3B,3C,3D,3E, 5A,5B,5C, and 7A,7B,7C,7D) may also be of value in patients with mycobacterial arthritis. In this regard, CT can be helpful in depicting early osseous erosion, intraarticular foreign bodies, and joint effusion. CT, however, is inherently suboptimal for enabling detection and evaluation of edema and associated periarticular soft-tissue changes. The presence and extent of inflammation can be accurately evaluated on MR imaging; MR imaging may allow more precise assessment of the bone marrow and soft-tissue involvement than CT. On MR images, mycobacterial arthritis displays intermediate to low signal intensity on T1-weighted images and high signal intensity on T2-weighted images in both the joint and adjacent bone [64, 66] (Figs. 3A,3B,3C,3D,3E and 5A,5B,5C).

Overall, both CT and MR imaging findings are nonspecific for atypical mycobacterial arthritis. The differential diagnosis generally includes different types of synovial arthropathy (e.g., tuberculous arthritis, pyogenic or fungal infections, rheumatoid arthritis, pigmented villonodular synovitis, idiopathic synovial osteochondromatosis), gout, calcium pyrophosphate dihydrate crystal deposition, regional osteoporosis, and idiopathic chondrolysis [11, 23, 64]. Synovial fluid aspiration and culture or biopsy of the synovial membrane are mandatory for definitive diagnosis are septic arthritis and identification of the infectious agent.


Soft-Tissue Manifestations
Top
 Introduction
 Epidemiologic Features
 Clinical Aspects
 Osteoarticular Manifestations
 Soft-Tissue Manifestations
Conclusion
 References
 
Cellulitis and Abscesses
Dermal inoculation of atypical mycobacteria may result in infection of the skin and subcutaneous soft tissues. If the infection is left untreated, cellulitis, cutaneous granulomas, and ulcers progress to shallow ulceration, suppuration, deep necrotizing infection, and scab formation [1, 7] (Fig. 5C). Localized, fluctuant soft-tissue abscesses and draining sinus tracts most commonly are associated with subjacent osteomyelitis. In the clinical setting of soft-tissue infection, local features include tenderness or pain, erythema, warmth, and skin swelling, whereas systemic signs such as fever, rigors, and malaise may be prominent [67].

Although cellulitis, ulcers, and abscesses can be diagnosed on the basis of clinical examination, imaging supplements diagnosis by documenting possible extension of infection into the deeper soft tissues and is particularly useful when the infection fails to resolve under adequate antibiotic therapy. In patients with cellulitis, for example, conventional radiographs show superficial soft-tissue swelling with streaky obliteration of the subcutaneous tissue layer [67]. CT can depict an alteration in the soft-tissue density and reveal the extent of the infectious process, but CT is rarely capable of distinguishing between different components of inflammation such as exudate and purulent material. Although controversial, 99mTC-methylene diphosphonate bone scanning may be useful in differentiating cellulitis from subjacent osteomyelitis. In patients with cellulitis, accumulation of the radionuclide in the infected area is increased during the angiographic and blood pool images of a three-phase bone scan, whereas in patients with osteomyelitis a focal increase in the accumulation of the radionuclide is evident in all three phases of the bone scan [68]. Additional study with 111In-labeled leukocytes may be helpful in differentiating cellulitis from osteomyelitis [58]. Cellulitis appears as diffuse areas of low signal intensity on T1-weighted and high signal intensity on T2-weighted spin-echo MR images within the inflamed soft tissues [50] (Figs. 3B, 3D, and 5C). After IV administration of gadolinium-containing contrast medium, avid enhancement of soft tissues is indicative of cellulitis.

As the infection progresses, pyogenic abscesses may form within the inflamed soft tissues. Although not routinely required, sonography, CT, and MR imaging may be worthwhile for detection and localization of an abscess [69]. MR imaging typically displays abscesses as loculated fluid collections that enhance peripherally after IV administration of gadolinium-containing contrast material [44, 57, 69]. Given the different patterns of contrast enhancement for each lesion, MR imaging is usually helpful in differentiating osteomyelitis from overlying cellulitis [50] or associated abscesses.

Septic Myositis
Septic myositis caused by atypical mycobacteria has recently been recognized in association with HIV infection and IV drug abuse [70]. Mycobacterial pyomyositis may also be observed in immunocompetent individuals after penetrating trauma or invasion from contiguous sites of infection. Clinical findings include fever, myalgia, erythema, local muscle swelling, "wooden" stiffness of the soft tissues, and fluctuance; septicemia may also result [67].

Advanced imaging, including sonography, CT, and MR imaging, is advocated to investigate infectious myositis. Among the findings encountered in the infectious process are prominent muscle swelling, effacement of the intramuscular and intermuscular fat planes, intramuscular abscesses, and adjacent soft-tissue edema. MR imaging may be of critical importance in the differential diagnosis of abscesses from myonecrosis, the latter occurring in association with IV drug abuse and HIV infection. Although both lesions show marginal contrast enhancement, myonecrosis, in contradistinction to muscular abscesses, is characterized by an absence of central high signal intensity on T2-weighted images. Radionuclide studies performed with gallium or indium may reveal additional distant abscesses [23]. The differential diagnosis of infectious myositis includes septic arthritis, osteomyelitis, deep venous thrombosis, soft-tissue sarcoma, and hematoma.

Septic Bursitis
Unlike tuberculosis, which may affect any bursa, atypical mycobacteria most commonly affect the superficial bursae over the knee (prepatellar bursa) and elbow (olecranon bursa) [7]. Because infection usually occurs by direct inoculation of the pathogen into the superficially situated subcutaneous bursa [23, 67], skin abrasion or laceration is usually present at the site of entrance. On physical examination, additional findings such as bursal tenderness, peribursal erythema, edema, and cellulitis are apparent.

Radiographic findings of atypical mycobacterial bursitis may be subtle and include subcutaneous edema, soft-tissue swelling, and, less frequently, minor calcification in the bursa or soft tissue. Chronically inflamed and distended bursae may be associated with erosion of the underlying bone caused by repetitive mechanical friction between bone and skin [41]. Sonography may conspicuously depict bursal infection and may guide fluid aspiration [65]. On MR images, bursitis appears as a well-circumscribed fluid collection [71]. Frequently, T1-weighted MR images may display foci of intermediate signal intensity because of septic debris [71] within the inflamed bursa. Infection of a bursa typically leads to thickening of its wall, which forms part of the abscess capsule. After IV administration of gadolinium-containing contrast material, MR imaging characteristically reveals marked enhancement of the wall of the inflamed bursa. Percutaneous bursal paracentesis and fluid aspiration and culturing may allow identification of the causative strain of atypical mycobacteria.

Septic Tenosynovitis
Most cases of tenosynovitis caused by atypical mycobacteria are located in the hand and wrist [7, 34, 72, 73], likely owing to both the relative abundance of synovium at these sites and the increased risk for pathogen inoculation through minor penetrating injuries at these sites [67]. Septic tenosynovitis may also occur in association with adjacent cellulitis. Infection may lead to tendon adhesions; however, penetration of the infection through the periosteum can lead to subjacent osteomyelitis, which may necessitate arthrodesis or amputation [74]. On rare occasions, suppuration, caseation of lesions, and eventually, extensive necrosis of the tenosynovium may occur [41]. Associated clinical features include pain, stiffness, swelling over the infected tenosynovium, and functional compromise of the hand [73].

Because any part of the tenosynovium of the hand may be involved in the infectious process, radiography may show soft-tissue swelling along the course of the involved tendon sheath; the flexor tendon sheaths, radioulnar bursae, and the dorsal wrist compartment may be affected [34, 67]. Typically, inflammatory changes of the tenosynovium include vascular engorgement, edema, cellular infiltration, and granulation tissue. On MR images, the inflamed tendon appears thickened and is surrounded by fluid. After IV administration of gadolinium-containing contrast material, prominent enhancement of the inflamed tendon sheath is evident. Sonography can also be used to detect fluid collections in the tendon sheath and to reveal thickening of the tendon itself.

Differential diagnosis of mycobacterial tenosynovitis includes pyogenic and fungal infection, giant cell tumor of the tendon sheath, rheumatoid arthritis, and pigmented villonodular synovitis. Because both sonographic and MR imaging findings are nonspecific for mycobacterial infection, it is imperative that aspiration of synovial fluid or biopsy of the inflamed synovial membrane be considered during the diagnostic workup.

Carpal Tunnel Syndrome
One characteristic manifestation of atypical mycobacterial tenosynovitis of the wrist is the carpal tunnel syndrome [72, 74], caused by an inflammation-related increase of the intracompartmental pressure. Clinical features include stiffness or swelling of the wrist, tingling of the affected fingers, or swelling of a single finger (sausage digit) [72].

On MR imaging, the median nerve appears enlarged and flattened, with increased signal intensity on T2-weighted and certain gradientecho images [75]. Occasionally, morphologic abnormalities with regard to the size and configuration of the median nerve or alterations in its signal intensity may be minimal; complementary MR techniques including IV administration of gadolinium-containing contrast agents and imaging after exercise of the wrist may be necessary. Eventually, catheterization of the carpal canal and measurement of intracompartmental pressure will document the correct diagnosis.


Conclusion
Top
 Introduction
 Epidemiologic Features
 Clinical Aspects
 Osteoarticular Manifestations
 Soft-Tissue Manifestations
 Conclusion
References
 
Delay in diagnosis of atypical mycobacterial infection is frequent and may be due not only to nonspecific clinical manifestations of disease, but also to a lack of familiarity of radiologists, pathologists, and other clinicians with these pathogens. Given the lack of specificity of imaging findings and clinical symptoms and signs, it becomes obvious that histopathologic analysis of biopsy specimens and mycobacterial culturing are crucial in establishing the diagnosis. The most commonly reported manifestations of atypical mycobacterial infections involving the musculoskeletal system are osteomyelitis, septic arthritis, cellulitis, abscess, septic myositis, septic bursitis, septic tenosynovitis, and carpal tunnel syndrome. All imaging examinations, particularly MR imaging, provide supplemental information that may be helpful for initiating early and correct therapeutic treatment.


References
Top
 Introduction
 Epidemiologic Features
 Clinical Aspects
 Osteoarticular Manifestations
 Soft-Tissue Manifestations
 Conclusion
 References
 

  1. Wolinsky E. Mycobacterial diseases other than tuberculosis. Clin Infect Dis 1992;15:1 -12[Medline]
  2. Peter G. Diseases caused by nontuberculous mycobacteria. In: Peter G, ed. Red book: report of the committee on infectious diseases, 24th ed. Elk Grove Village, IL: American Academy of Pediatrics, 1997:563 -567
  3. Toossi Z, Ellner J. Mycobacterium tuberculosis and other mycobacteria. In: Gorbach S, Bartlett J, Blacklow N, eds. Infectious diseases, 2nd ed. Philadelphia: Saunders, 1998: 2299-2307
  4. Spitznagel J. Mycobacteria: tuberculosis and leprosy. In: Schaechter M, Engleberg N, Eisenstein B, Medoff G, eds. Mechanisms of microbial disease, 3rd ed. Baltimore, MD: Williams & Wilkins, 1998:230 -242
  5. Iseman M, Huitt G. Nontuberculous mycobacterial infections. In: Gorbach S, Bartlett J, Blacklow N, eds. Infectious diseases, 2nd ed. Philadelphia: Saunders, 1998: 1513-1528
  6. Iseman M. Mycobacterium avium complex and the normal host. N Engl J Med 1989;321:896 -898[Medline]
  7. Wolinsky E. Nontuberculous mycobacteria and associated diseases. Am Rev Respir Dis 1979;119:107 -159[Medline]
  8. Good R, Snider D Jr. Isolation of nontuberculous mycobacteria in the United States, 1980. J Infect Dis 1982;146:829 -833[Medline]
  9. O'Brien R, Geiter L, Snider D. The epidemiology of nontuberculous mycobacterial diseases in the United States: results from a national survey. Am Rev Respir Dis 1987;135:1007 -1014[Medline]
  10. Chapman M, Murray R, Stocker D. Tuberculosis of the bones and joints. Semin Roentgenol 1979;14:266 -288[Medline]
  11. Resnick D, Niwayama G. Osteomyelitis, septic arthritis, and soft tissue infection: organisms. In: Resnick D, ed. Diagnosis of bone and joint disorders, 3rd ed. Philadelphia: Saunders, 1995: 2448-2558
  12. Raszka W, Skillman L, McEvoy P, Robb M. Isolation of nontuberculous, non-avium mycobacteria from patients infected with human immunodeficiency virus. Clin Infect Dis 1995;20:73 -76[Medline]
  13. Perandones C, Roncoroni A, Frega N, Bianchini H, Hübscher O. Mycobacterium gastri arthritis: septic arthritis due to Mycobacterium gastri in a patient with a renal transplant. J Rheumatol 1991;18:777 -778[Medline]
  14. Department of Health. Tuberculous notifications in New South Wales 1989. New South Wales, Australia: Department of Health, 1989. State Health Publication 89-086
  15. Woods G, Washington J. Mycobacteria other than Mycobacterium tuberculosis: review of microbiologic and clinical aspects. Rev Infect Dis 1987;9:275 -294[Medline]
  16. Wallace R, Brown B, Onyi G. Skin, soft tissue, and bone infections due to Mycobacterium chelonae: importance of prior corticosteroid therapy, frequency of disseminated infections, and resistance to oral antimicrobials other than clarithromycin. J Infect Dis 1992;166:405 -412[Medline]
  17. Fraser R, Pare J, Pare P, et al. Diagnosis of diseases of the chest, 3rd ed. Philadelphia: Saunders, 1990: 933-941
  18. Miller W, Miller W Sr. Pulmonary infections with atypical mycobacteria in the normal host. Semin Roentgenol 1993;28:139 -149[Medline]
  19. Woodring J, Vandiviere H. Pulmonary disease caused by nontuberculous mycobacteria. J Thorac Imaging 1990;5:64 -76[Medline]
  20. Montessori V, Phillips P, Montaner J, Haley L, Bessuille E, Black W. Species distribution in human immunodeficiency virus-related mycobacterial infections: implications for selection of initial treatment. Clin Infect Dis 1996;22:989 -992[Medline]
  21. Volk W, Gerbhardt B, Hammarskjold M, Kadner R. Atypical mycobacteria. In: Volk W, Gerbhardt B, Hammarskjold M, Kadner R, eds. Essentials of medical microbiology, 5th ed. Philadelphia: Lippincott-Raven, 1996:429 -439
  22. Jenkin D, Dall G. Lesions of bone in disseminated infection due to the Mycobacterium avium-intracellulare group. J Bone Joint Surg Br 1975;57-B:373 -375
  23. Resnick D, Niwayama G. Osteomyelitis, septic arthritis, and soft tissue infection: mechanisms and situations. In: Resnick D, ed. Diagnosis of bone and joint disorders, 3rd ed. Philadelphia: Saunders, 1995:2325 -2418
  24. Savage RA. Atypical mycobacteria in bone marrow histiocytes. JAMA 1986;255:1192[Medline]
  25. Marchevsky A, Damsker B, Green S, Tepper S. The clinicopathological spectrum of nontuberculous mycobacterial osteoarticular infections. J Bone Joint Surg Am 1985;67-A:925 -929[Abstract/Free Full Text]
  26. Klah E, Jensen D, Meyer P. Pathology of Mycobacterium avium-intracellulare infection in acquired immunodeficiency syndrome. Hum Pathol 1987;18:709 -714[Medline]
  27. Cohen R, Samoszuk M, Busch D, Lagios M. Occult infections with M. intracellulare in bonemarrow biopsy specimens from patients with AIDS. N Engl J Med 1983;308:1475 -1476[Medline]
  28. Barton A, Bernstein M, Struthers J, O'Neill T. Mycobacterium marinum infection causing septic arthritis and osteomyelitis. Br J Rheumatol 1997;36:1207 -1209[Abstract/Free Full Text]
  29. Williams C, Rjordan D. Mycobacterium marinum infections of the hand. J Bone Joint Surg Am 1973;55-A:1042 -1050[Abstract/Free Full Text]
  30. Alloway J, Evangelisti S, Sartin J. Mycobacterium marinum arthritis. Semin Arthritis Rheum 1995;24:382 -390[Medline]
  31. Hofer M, Hirschel B, Kirshner P, et al. Brief report: disseminated osteomyelitis from Mycobacterium ulcerans after a snakebite. N Engl J Med 1993;328:1007 -1009[Free Full Text]
  32. Ellner J, Goldberger M, Parenti D. Mycobacterium avium infection and AIDS: a therapeutic dilemma in rapid evolution. J Infect Dis 1991;163:1326 -1335[Medline]
  33. Mahowald M, Messner R. Atypical mycobacterial infections in bones and joints. In: Schlossberg D, ed. Orthopedic infection, 1st ed. New York: Springer-Verlag, 1988: 78-82
  34. Kelly P, Weed L, Lipscomb P. Infections of tendon sheaths, bursae, joints and soft tissues by acid-fast bacilli other than tubercle bacilli. J Bone Joint Surg Am 1963;45-A:327 -336[Abstract/Free Full Text]
  35. Rougraff B, Reeck C, Slama T. Mycobacterium terrae osteomyelitis and septic arthritis in a normal host. Clin Orthop 1989;238:308 -310
  36. Wolfgang G. Tuberculosis joint infection. Clin Orthop 1978;136:257 -263
  37. Edwards M, Huber T, Baker C. Mycobacterium terrae synovitis and osteomyelitis. Am Rev Respir Dis 1978;117:161 -163[Medline]
  38. Solheim L, Kjelsberg F. Recurrent mycobacterial osteomyelitis: report of a case due to Mycobacterium avium-intracellulare-scrofulaceum complex and BCG inoculation. Arch Orthop Trauma Surg 1982;102:277 -280
  39. Hing D, Delohery J, Abbot M. Multifocal osteomyelitis caused by Mycobacterium chelonei. Med J Aust 1983;1:529 -531[Medline]
  40. Feldman F, Auerbach R, Johnston A. Tuberculous dactylitis in the adult. Am J Roentgenol Radium Ther Nucl Med 1971;112:460 -479[Medline]
  41. Norden C, Gillespie W, Nade S. Mycobacterial infections of the musculoskeletal system. In: Norden C, Gillespie W, Nade S, eds. Infections in bones and joints. Boston: Blackwell Scientific, 1994:211 -230
  42. Gillespie W, Nade S. Mycobacterial infections. In: Gillespie W, Nade S, eds. Musculoskeletal infections. Melbourne: Blackwell Scientific, 1987:323 -358
  43. Miller W, Perkins M, Richardson W, Sexton D. Pott's disease caused by Mycobacterium xenopi: case report and review. Clin Infect Dis 1994;19:1024 -1028[Medline]
  44. Sharif H, Morgan J, Shahed M, Al Thagafi M. Role of CT and MR imaging in the management of tuberculous spondylitis. Radiol Clin North Am 1995;33:787 -804[Medline]
  45. Resnick D, Niwayama G. Osteomyelitis, septic arthritis, and soft tissue infection: axial skeleton. In: Resnick D, ed. Diagnosis of bone and joint disorders, 3rd ed. Philadelphia: Saunders, 1995: 2419-2447
  46. Jain R, Sawhney S, Berry M. Computed tomography of vertebral tuberculosis: patterns of bone destruction. Clin Radiol 1993;47:196 -199[Medline]
  47. Berquist T, Brown M, Fitzerald R, et al. Magnetic resonance imaging applications in musculoskeletal infection. Magn Reson Imaging 1985;3:219 -230[Medline]
  48. Mason M, Zlatkin M, Esterhai J, et al. Chronic complicated osteomyelitis of the lower extremity: evaluation with MR imaging. Radiology 1989;173:355 -359[Abstract/Free Full Text]
  49. Beltran J, Noto A, McGhee R, et al. Infections of the musculoskeletal system: high-field-strength MR imaging. Radiology 1987;164:449 -454[Abstract/Free Full Text]
  50. Unger E, Moldofsky P, Gatenby R, Hartz W, Broder G. Diagnosis of osteomyelitis by MR imaging. AJR 1988;150:605 -610[Abstract/Free Full Text]
  51. Modic M, Pflanze W, Feiglin D, et al. Magnetic resonance imaging of musculoskeletal infections. Radiol Clin North Am 1986;24:247 -258[Medline]
  52. Erdman W, Tamburro F, Jayson H, et al. Osteomyelitis: characteristics and pitfalls of diagnosis with MR imaging. Radiology 1991;180:533 -539[Abstract/Free Full Text]
  53. Tang J, Gold R, Bassett L, et al. Musculoskeletal infection of the extremities: evaluation with MR imaging. Radiology 1988;166:205 -209[Abstract/Free Full Text]
  54. Smith AS, Weinstein MA, Mizushima A, et al. MR imaging characteristics of tuberculous spondylitis vs vertebral osteomyelitis. AJR 1989;153:399 -405[Abstract/Free Full Text]
  55. Hoffman E, Crosier J, Cremin B. Imaging in children with spinal tuberculosis. J Bone Joint Surg Br 1993;75-B:233 -239
  56. de Roos A, van Persijn van Meerten EL, Bloem JL, Bluemm RG. MRI of tuberculous spondylitis. AJR 1986;147:79 -82[Abstract/Free Full Text]
  57. Wall SD, Fisher MR, Amparo EG, Hricak H, Higgins CB. Magnetic resonance imaging in the evaluation of abscesses. AJR 1985;144:1217 -1221[Abstract/Free Full Text]
  58. Schauwecker D. Osteomyelitis: diagnosis with In-111-labeled leukocytes. Radiology 1989;171:141 -146[Abstract/Free Full Text]
  59. Hayes C, Conway W, Sundaram M. Misleading aggressive MR imaging appearance of some benign musculoskeletal lesions. RadioGraphics 1992;12:1119 -1134[Abstract]
  60. Marinelli D, Albelda S, Williams T, et al. Nontuberculous mycobacterial infection in AIDS: clinical, pathologic, and radiographic features. Radiology 1986;160:77 -82[Abstract/Free Full Text]
  61. Cheatum D, Hudman V, Jones S. Chronic arthritis due to Mycobacterium intracellulare. Arthritis Rheum 1976;19:777 -781[Medline]
  62. Haywood T, Williamson S. Radiographic findings of extremity tuberculosis in childhood: back to the future? RadioGraphics 1994;14:561 -570[Abstract]
  63. Blumenthal D, Zucker J, Hawkins C. Mycobacterium avium complex-induced septic arthritis and osteomyelitis in a patient with the acquired immunodeficiency syndrome. Arthritis Rheum 1990;33:757 -758[Medline]
  64. Whitaker M, Jelinek J, Kransdorf M, et al. Case report 653: arthritis of the wrist due to Mycobacterium avium-intracellulare. Skeletal Radiol 1991;20:291 -293[Medline]
  65. Marchal G, Van Holsbeeck E, Raes M, et al. Transient synovitis of the hip in children: role of US. Radiology 1987;162:825 -828[Abstract/Free Full Text]
  66. Araki Y, Tsukaguchi I, Shino K, et al. Tuberculous arthritis of the knee: MR findings. (letter) AJR 1993;160:664
  67. Gillespie W, Nade S. Soft tissue infections (myositis and cellulitis, bursitis, tenosynovitis). In: Gillespie W, Nade S, eds. Musculoskeletal infections. Melbourne: Blackwell Scientific Publications, 1987:303 -322
  68. Gilday D, Paul D, Paterson J. Diagnosis of osteomyelitis in children by combined blood pool and bone imaging. Radiology 1975;117:331 -335[Abstract]
  69. Greenberg R, Poepsel P, Reynaud S, et al. Staphylococcal infection of fascial space diagnosed by ultrasonography. South Med J 1983;76:814[Medline]
  70. Wolf R, Sprenger H, Mooyaart E, et al. Nontropical pyomyositis as a cause of subacute, multifocal myalgia in the acquired immunodeficiency syndrome. Arthritis Rheum 1990;33:1728 -1732[Medline]
  71. Rutten M, Van den Berg J, Van den Hoogen, et al. Nontuberculous mycobacterial bursitis and arthritis of the shoulder. Skeletal Radiol 1998;27:33 -35[Medline]
  72. Stratton C, Phelps D, Reller L. Tuberculous tenosynovitis and carpal tunnel syndrome caused by Mycobacterium szulgei. Am J Med 1978;65:349 -351[Medline]
  73. Chow S, Ip F, Lau J, et al. Mycobacterium marinum infection of the hand and wrist. J Bone Joint Surg Am 1987;69-A:1161 -1168[Abstract/Free Full Text]
  74. Lacy J, Viegas S, Calhoun J, et al. Mycobacterium marinum flexor tenosynovitis. Clin Orthop 1989;238:288 -293
  75. Resnick D. Carpal tunnel abnormalities. In: Resnick D, ed. Diagnosis of bone and joint disorders, 3rd ed. Philadelphia: Saunders, 1995:2928 -2930

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