Abstract
Tuberculosis can lead to serious destruction of musculoskeletal structures such as the bones, joints, and soft tissues. Early diagnosis of musculoskeletal tuberculosis is important in order to minimize structural damage and prevent permanent complications. The diagnosis requires a high degree of awareness as the clinical presentation may be indolent, non-specific, and may mimic other disease processes. Tissue destruction from tuberculous granulomas produces some characteristic patterns which can be demonstrated by imaging studies. Radiography, ultrasound imaging, computed tomography, and magnetic resonance imaging help in detection of the disease, guide appropriate laboratory investigation and surgical management, as well as in the evaluation of treatment outcome. Whole-body [Fluorine-18]-fluoro-2-deoxy-d-glucose positron-emission tomography has a gradually increasing role in the detection of multifocal lesions and disease monitoring. Knowing the characteristic imaging features and potential mimics aids in timely diagnosis and treatment of musculoskeletal tuberculosis.
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Keywords
- Bone infection
- Bone tuberculosis
- Infectious tenosynovitis
- Joint infection
- Musculoskeletal infection
- Musculoskeletal tuberculosis
- Osteomyelitis
- Septic arthritis
- Tuberculous arthritis
- Tuberculous osteomyelitis
- Tuberculous tenosynovitis
1 Introduction
Musculoskeletal tuberculosis (TB) is an important cause of mortality and morbidity worldwide. Cases are rising because of the steadily increasing number of immunocompromised hosts such as patients with human immunodeficiency virus (HIV) infection, immunosuppressive treatment, advanced age, and also a rise in immigration from countries with a high disease prevalence (Arora and Chopra 2019; Suarez et al. 2019; World Health Organization 2021). Appendicular involvement, although less common than spinal TB, can lead to serious bone and joint destruction. The indolent and diverse clinical presentation often mimics many other diseases, and may cause a delay in diagnosis. The emergence of multidrug-resistant strains increases the difficulty in treatment and control of disease spread. Early imaging diagnosis plays an important role in directing appropriate laboratory investigation, hence allowing timely diagnosis and treatment.
2 Pathophysiology
TB affects the musculoskeletal system, causing osteomyelitis, arthritis, or soft tissue infection. The organism reaches the musculoskeletal system via hematogenous spread or by direct inoculation. Hematogenous spread is more common and will be discussed in more detail in the following paragraphs. The disease either presents during the primary spread of the organism or as a reactivation, usually when host immunity decreases. At the site of infection, the TB bacilli induce a granulomatous inflammatory reaction that consists of epithelioid cells, lymphocytes, and multinucleated giant cells, forming either caseating or noncaseating granulomas (Natarajan et al. 2020). The host inflammatory response results in liquefactive and caseous necrosis, tissue destruction, and abscess formation. The infective focus then spreads to the surrounding structures. In the late stage of the disease, the granulomatous lesions may calcify (Sharma et al. 1978).
The metaphysis of long bones and large weight-bearing joints, such as the hip and knee, are commonly affected because of their rich vascular supply (Pigrau-Serrallach and Rodríguez-Pardo 2013; Natarajan et al. 2020). The predilection for the location of osteomyelitis depends on the distribution of intraosseous vascular structures according to age. In infants younger than 1.5 years of age, transphyseal spread is common, due to vessels crossing the growth plate. In children aged between one and 16 years, the metaphysis is the most common site, as the epiphyseal growth plate acts as a natural barrier to the spread of infection. However, isolated epiphyseal lesions may still occur, owing to the presence of the nutrient artery of the epiphysis. In adults, vascular distribution in form of communicating metaphyseal and epiphyseal vessels allows the infection to reach subchondral bone (Wang et al. 1999; Resnick 2002a; Ranson 2009) (Fig. 1).
Tuberculous arthritis may result from primary spread via subsynovial vessels, or be secondary to osteomyelitis or infected para-articular tissue (De Backer et al. 2006) (Fig. 2). As the exudative fluid in tuberculous arthritis lacks proteolytic enzymes, the cartilage is usually spared until later stages of the disease (Akeson et al. 2002). The pattern of cartilage destruction reflects the growth of granulation tissue which can be along the free surface of cartilage, between the cartilage and subchondral bone, or result from penetration through the cartilage (Resnick 2002b) (Fig. 2).
Soft tissue infections, including pyomyositis, bursitis, tenosynovitis, and subcutaneous tissue abscesses, can present as a primary affected site but is more commonly a complication of osteomyelitis or arthritis. Tuberculous tenosynovitis and bursitis initially develop as a serous effusion, followed by synovial thickening, and accumulation of tissue debris and caseous material. Eventually, debris and synovial thickening become prominent and there is minimal effusion. Tenosynovitis may lead to tendon tethering or rupture (Jaovisidha et al. 1996).
3 Clinical Features and Complications
Musculoskeletal TB is a disease that affects all age groups but there is a predilection for children and the elderly (Perez-Velez and Marais 2012; Arora and Chopra 2019). Clinical features of musculoskeletal TB are variable and non-specific. Infected patients can present with chronic pain, limb deformity, dislocation, pathological fracture, palpable mass as a result of abscess formation, or draining skin sinus. Fever is infrequent and is mostly associated with disseminated infection (Naidoo et al. 2017). Multifocal lesions occur in 7–11% of patients and are commonly associated with HIV infection, children, or poor physical status (Prasad et al. 2012; Pigrau-Serrallach and Rodríguez-Pardo 2013; Naidoo et al. 2017; Suarez et al. 2019). Not all lesions are symptomatic, and different stages of destruction and healing can be expected as a result of multiple episodes of hematogenous seeding of the organism and variable local tissue immunity.
The major predisposing factors of musculoskeletal TB are conditions leading to immunosuppression, caused by diseases or treatment (Hodkinson et al. 2009; Lin et al. 2009). Tissue injury, either by trauma or surgery, is a predisposing factor because of increased vascular supply and impairment of the local immune system. Tuberculous infection has been reported following different types of surgery such as fracture fixation (Kumar et al. 2006), reconstruction of the anterior cruciate ligament of the knee (Nag et al. 2009), and sternotomy (Gopal et al. 2007). Inflammatory joint disease may also predispose to tuberculous arthritis (Bryan et al. 1982; Hortas et al. 1988). Prosthetic joint infection due to TB is uncommon. Three pathogenic mechanisms have been reported: (1) Active tuberculous arthritis present at the time of surgery but not known to clinician; (2) Hematogenous spread from a distant focus; and (3) Surgical trauma resulting in activation of previous unknown TB (Hugate and Pellegrini 2002; Khater et al. 2007; Carrega et al. 2013; Harwin et al. 2013).
Bone and joint infections often subsequently progress to soft tissue abscesses. Tuberculous abscess typically has a minimal inflammatory response, and is also called a cold abscess. If untreated, the soft tissue abscess may form a sinus tract which drains to the skin. In the immature skeleton, bone and joint tuberculosis may cause limb length discrepancy and deformity. In tenosynovitis of the wrist, thickened synovial tissue and debris can envelop the median nerve, resulting in the carpal tunnel syndrome (Hassanpour and Gousheh 2006).
4 Imaging Features
4.1 Radiography
Radiographs are the main modality used in the detection of musculoskeletal infection. Due to the typically late and indolent clinical presentation, radiographs commonly reveal the advanced stages of disease with considerable structural destruction. The features of tuberculous osteomyelitis are a well-defined osteolytic lesion usually located in the metaphysis of long bones with or without sclerotic reaction, cortical expansile remodeling, sequestrum, and periostitis. Transphyseal spread is a characteristic feature of tuberculous osteomyelitis, a finding which is unusual for bacterial infection (De Vuyst et al. 2003) (Figs. 3, 4, and 5). An isolated epiphyseal lesion resulting from epiphyseal vessel spread may sometimes occur (Fig. 6)
Multifocal tuberculous osteomyelitis, also called osteitis cystica tuberculosa multiplex, is an unusual form of osteomyelitis that occurs in children more often than in adults (Shikhare et al. 2011). The disease manifests radiographically as well-defined osteolytic lesions resembling bone cysts of variable sizes. Sclerotic changes at the lesion margins are usually minimal and when present support evidence of healing (Tiwari et al. 2007) (Fig. 7).
Tuberculous dactylitis or osteomyelitis of the short tubular bone of hands and feet commonly occurs in younger patients, particularly children aged less than 6 years (Ranjan et al. 2019). These patients often present with soft tissue swelling and flexion deformity. Characteristic radiographic features include an osteolytic lesion, fusiform expansion of the bone and thick periosteal reaction, leading to the term spina (short bone) ventosa (inflated with air) (Fig. 8). In the mild form of the disease, dactylitis causes soft tissue swelling and periosteal reaction.
The radiographic hallmark of tuberculous arthritis, described as the Phemister triad, consists of marginal bone erosions, juxta-articular osteoporosis, and relatively preserved joint space (Phemister and Hatcher 1933) (Figs. 9, 10, and 11). Large subchondral bone destruction, due to intraosseous abscesses, may be present (Fig. 10). Widespread disease may also occur in the interconnecting joints of the wrist and midfoot (Dhillon and Nagi 2002; Hsu et al. 2004) (Fig. 11). Soft tissue abscesses, tenosynovitis, or bursitis can lead to a large soft tissue mass detectable on radiographs (Fig. 10a). Associated soft tissue calcification is a suggestive sign of tuberculous infection (Sharma et al. 1978) (Fig. 12).
Apart from structural damage by granulomatous formation, radiographs can demonstrate complications such as pathological fracture (Fig. 13), dislocation (Figs. 14 and 15), limb length discrepancy, and deformities. Enlarged epiphyses result from reactive hyperemia affecting the growing ossification center (Fig. 7b). In the hip, gradual joint destruction in the weight-bearing joint causes bone remodeling and acetabular protrusion (Fig. 16a). Fibrous ankylosis occurs as an end-stage of the disease (De Vuyst et al. 2003). Bony ankylosis is uncommon in tuberculosis except in cases with surgical intervention (Parsa et al. 2018).
4.2 Computed Tomography
Computed tomography (CT) helps better demonstrate the features of TB detected by radiographs, particularly bone erosions, sequestrum (Fig.10b–d), pyomyositis, and soft tissue calcification (Figs. 15b, c and 17). CT enables detailed evaluation of abscess extension, internal organ involvement, and disseminated disease (Fig. 18). CT is particularly useful in the assessment of chest wall infection, which has a predilection for the sternal margin because of spread of infection via the internal mammary lymph nodes (Bergeron et al. 2017) (Fig. 19a). Other affected sites are the sternoclavicular joint, costochondral junction, rib shafts, and costovertebral joints (Morris et al. 2004). Mediastinal extension is well demonstrated by CT (Fig. 20). CT is also useful for guiding biopsy.
4.3 Magnetic Resonance Imaging
Magnetic resonance imaging (MRI) is the most useful modality for the evaluation of musculoskeletal TB, as it provides a good demonstration of inflammatory processes in bones, joints, and soft tissues (Figs. 5b, 9b–d, and 19b, c). The minimal inflammatory response of the tissues around an abscess is a characteristic finding of tuberculous infection (Fig. 21). Sinus formation is seen as “tram-track” enhancement extending from the infected site to the skin (Figs. 14c, d and 22). In children, MRI allows better evaluation of transphyseal spread, articular involvement, and infection of the unossified part of the epiphysis (Figs. 5b and 23).
A characteristic sign of abscess formation on MRI is the presence of a penumbra, which refers to the T1-hyperintense wall of abscess representing vascularized granulation tissue (Grey et al. 1998) (Fig. 23). This penumbra sign has a high specificity (96%) for chronic abscesses and helps in differentiating musculoskeletal infection from tumors (McGuinness et al. 2007). However, the sign is not specific to TB, and abscess formation from other organisms can also produce this sign. Rarely, this sign has also been reported in chondrosarcoma, eosinophilic granuloma, fibrous dysplasia, pigmented villonodular synovitis, and benign cystic lesions (Grey et al. 1998; McGuinness et al. 2007).
In tuberculous arthritis, MRI can demonstrate the cartilage and bone destruction caused by granulation tissue. With the lack of proteolytic enzymes, focal areas of relatively intact cartilage may be present between the areas of granulation tissue (Fig. 9d). Synovial proliferation with heterogeneous intermediate to hypointense signal on T2-weighted images is found in approximately 40% of tuberculous arthritis (Sawlani et al. 2003) (Fig. 16b). Tissue components in caseous necrosis, including fibrosis, macrophage infiltration, and free radicals from macrophage by-products, contribute to T2-hypointense signal in tuberculous synovitis (Suh et al. 1996; Sawlani et al. 2003) (Fig. 16b). Presence of rice bodies in the joint, bursa, or tendon sheath is a sign of chronic synovitis, a feature also sometimes seen in tuberculous infection. Rice bodies have been described in various rheumatic diseases including rheumatoid arthritis, juvenile idiopathic arthritis, or osteoarthritis (Griffith et al. 1996; Forse et al. 2012; Subramaniam et al. 2012). Rice bodies represent debris whose shape resembles grains of rice, and consists of fibrin collagen and mononuclear cells (Popert 1985) (Fig. 24).
4.4 Ultrasound Imaging
Ultrasound (US) imaging is a good modality for the detection of joint effusion, synovial thickening, bone erosion, and soft tissue extension. There is often very marked synovial thickening which contrasts with low volume joint effusion. Para-articular abscess, rice bodies, and granulomatous calcifications are well detected (Fig. 25). US imaging can also be used for guiding fluid aspiration.
4.5 Nuclear Medicine Imaging
Nuclear medicine imaging studies allow detection of multifocal infection and monitoring of disease but its utility limited by low specificity. Three-phase 99Mtechnetium (Tc) methylene diphosphonate (MDP) bone scintigraphy is positive in active and healing osteomyelitis. Gallium scintigraphy and labeled leukocyte imaging help identification of active infection (Palestro et al. 2006). Whole-body [Fluorine-18]-fluoro-2-deoxy-d-glucose positron-emission tomography (18F-FDG PET) has a gradually increasing role in detecting multifocal lesions, assessing disease activity, and monitoring response to treatment (Ankrah et al. 2016). Active TB has avid tracer uptake (Fig. 26). Since 18F-FDG is a non-specific tracer, it may cause a false-positive diagnosis in patients being evaluated for tumor metastasis.
5 Imaging Differential Diagnosis
5.1 Tuberculous Osteomyelitis
Intraosseous abscesses cause well-defined osteolytic lesions mimicking tumor or tumor-like conditions such as simple bone cyst, aneurysmal bone cyst, chondroblastoma, or intraosseous tophi. Multifocal tuberculous osteomyelitis shares similar imaging features with eosinophilic granuloma, bone metastases, and multiple myeloma. The differential diagnosis of tuberculous dactylitis includes other conditions affecting short tubular bones such as vaso-occlusive insult of sickle cell disease, eosinophilic granuloma, and enchondroma (Ejindu et al. 2007; Ranjan et al. 2019). Tuberculous osteomyelitis of the femoral capital epiphysis in children can cause flattening and sclerotic changes, with an imaging appearance similar to Perthes disease (Agarwal 2020) (Fig. 5c). Presence of abscess formation, penumbra sign, and track-like transphyseal spread help in distinguishing abscesses from other conditions.
5.2 Tuberculous Arthritis
The clinical and radiological appearances of pyogenic arthritis and inflammatory arthritis share some similar features with tuberculous arthritis. Bone erosions, subchondral bone marrow edema, and inflammatory changes of the surrounding soft tissues due to pyogenic arthritis are more prominent than those of TB. The abscess walls in TB tend to be smooth and thin, while they are typically irregular and thick in pyogenic arthritis (Hong et al. 2001). Although rare, coexistent TB and pyogenic arthritis have been reported (Dojode et al. 2018). The main presumptive imaging signs of tuberculous arthritis are summarized in Table 1.
Rheumatoid arthritis typically presents as a symmetrical polyarticular disease. However, the disease may initially manifest as a monoarticular involvement and persist in that stage for a long time. Both rheumatoid and tuberculous arthritis can cause juxta-articular osteoporosis and heterogeneous T2-hypointense synovitis. Synovitis related to rheumatoid arthritis tends to be uneven and thick, while tuberculous synovitis is smooth and thin. Large bone erosions and para-articular abscesses favor tuberculosis (Choi et al. 2009).
The destruction pattern of TB in the foot may mimic neuropathic joint disease. Tuberculous arthritis, particularly in the interconnected joints of midfoot, has potential for widespread destruction, similar to the pattern seen in neuropathic joint disease. In contrast to neuropathic joint, severe osteoporosis is the hallmark of tuberculous arthritis during the active stage (Dhillon and Nagi 2002). The presence of para-articular abscesses and draining sinus leads to the diagnosis of infectious arthritis (Zacharia et al. 2003) (Fig. 27).
On MRI, synovial chondromatosis manifests as intra-articular loose bodies with hypointense signal on T2-weighted images, similar to that of rice bodies. However, on T1-weighted images, the signal intensity of synovial chondromatosis loose bodies is hyperintense, while that of rice bodies of TB are almost imperceptible (Chen et al. 2002) (Fig. 28).
5.3 Tuberculous Soft Tissue Infection
Tuberculous myositis and bursitis can present as a slow-growing mass that clinically simulates a tumor (Batra et al. 2007). Infection tends to spread along the low resistant space under the fascia (Soler et al. 2001). CT, MRI, and US imaging allow detection of the abscess and evaluation of the extent of disease. The calcification of granulomatous tissue at the wall of abscesses is characteristic of TB, but can also be a feature of other chronic bacterial infections (Coppola et al. 1987; Pattamapaspong and Muttarak 2011). Tuberculous abscesses of the anterior chest wall can be clinically confused with breast masses (Chung et al. 1996; Arslan et al. 1999; Jain et al. 2009; Teo et al. 2009) (Fig. 20). CT and MRI help confirm the precise location of the disease.
6 Diagnosis Confirmation
The definite diagnosis of musculoskeletal TB requires positive culture or smear microscopy from pus or infected tissue. However, smear microscopy has a low sensitivity (less than 40%), causing difficulty in diagnosis (Natarajan et al. 2020). Culture may yield 80% sensitivity but takes 6–8 weeks, resulting in a delay of treatment and potential further structural damages (Gardam and Lim 2005). Molecular methods examining for the presence of M. tuberculosis-specific DNA in biopsy and cytology specimens provide timely reliable diagnostic results and early identification of drug-resistant strains (Ghanekar et al. 2019; Natarajan et al. 2020). The histopathological findings of granulomatous and necrotizing inflammatory reaction, although non-specific, help suggest the diagnosis of TB. Infected specimens should be taken from the depth of the infected site to avoid contamination by other organisms at the sinus tract. In endemic areas or in patients with a risk of exposure to TB, diagnosis that is based on the combination of clinical, imaging, and histopathological findings is practically acceptable (Ghanekar et al. 2019).
7 Treatment
Musculoskeletal TB is typically treated using anti-TB drugs. The optimal treatment duration remains debatable but a 9–12 month course is recommended (Nahid et al. 2016). Surgical intervention aims to facilitate healing, prevent the spread of the infection, and maintain function. If performed, debridement needs to include sinus tracts which may not be possible by the standard incision; thus imaging plays a role in surgical planning (Dhillon et al. 2017). Arthrodesis or arthroplasty may be necessary in order to relieve pain and maintain function. Surgery can provide successful outcome when combined with adequate anti-TB drug treatment (Dhillon et al. 2017; Parsa et al. 2018).
The response to treatment is judged by clinical and radiological improvement. Clinically, fever, night sweats, weight loss, and draining sinuses should resolve. Radiological signs of healing include resolution of abscesses and bone marrow edema, with gradual remineralization of affected bones. No improvement or deterioration of the disease after five months of treatment should raise the concern of treatment failure. Follow-up for at least 2 years after completing the course of treatment is recommended for monitoring of possible disease relapse (World Health Organization and Ministry of Health and Family Welfare, Government of India 2016).
8 Conclusion
Extraspinal musculoskeletal TB has various clinical manifestations and imaging findings, depending on whether the affected sites are the bone, joint, or soft tissues. Imaging studies are valuable tools in lesion detection and achieving an accurate diagnosis, bearing in mind that TB can mimic a number of other musculoskeletal diseases. Although non-specific, certain patterns of structural destruction accompanied by abscesses with minimal inflammatory reaction, soft tissue calcification and sinus tracts are suggestive of TB. When combined with the appropriate clinical context, these characteristic imaging features lead to timely diagnosis and appropriate treatment.
Abbreviations
- CT:
-
Computed tomography
- MRI:
-
Magnetic resonance imaging
- TB:
-
Tuberculosis
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Pattamapaspong, N., Peh, W.C.G. (2022). Imaging of Extraspinal Musculoskeletal Tuberculosis. In: Ladeb, M.F., Peh, W.C.G. (eds) Imaging of Tuberculosis. Medical Radiology(). Springer, Cham. https://doi.org/10.1007/978-3-031-07040-2_13
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DOI: https://doi.org/10.1007/978-3-031-07040-2_13
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