Osseous Manifestations of Tuberculosis in Children.9

Osseous Manifestations of Tuberculosis in Children

Mahomed Noor Rasool, F.C.S.(SA)Orth

Study conducted at King Edward VIII Hospital, Durban, South Africa

Summary: Forty-two children with tuberculous osteomyelitiswere seen and treated between 1984 and 1999. The age rangedfrom 1 to 12 years (average 6); there were 31 boys and 11 girls.There were 50 osseous lesions (excluding spinal and synovial).Five children had multifocal bone involvement. There werefour basic types of lesions: cystic (n � 26), infiltrative (n �10), focal erosions (n � 8), and spina ventosa (n � 6). Themajority of the lesions were in the metaphyses (n � 25); theremainder were in the diaphysis, epiphysis, short tubular bones,

flat bones, and small round bones. The erythrocyte sedimenta-tion rate was normal in seven, and the Mantoux test was nega-tive in four. Bone lesions resembled pyogenic and fungal in-fections and benign and malignant bone tumors. Histologicconfirmation was obtained in all patients. Curettage and anti-tuberculous treatment yielded good results in the majority ofpatients, with follow-up of 6 months to 9 years. Biopsy ismandatory to confirm the diagnosis. Key Words: Osseous tu-berculosis—Radiologic spectrum.

Tuberculosis remains a major cause of skeletal infec-tion in many developing countries. Since 1985, somedeveloped countries have recorded a resurgence in theincidence of skeletal tuberculosis. This increase has beenattributed to acquired immunodeficiency syndrome(AIDS), homelessness, a decline in tuberculosis controlprograms, immigration, and intravenous drug abuse (26,28,30,32). In other countries, bone lesions have beenreported to be related to Bacille Calmette-Guérin (BCG)immunization (4,19,29).

Historically, the bone lesions of tuberculosis were pre-dominantly of the multifocal and disseminated type (Jun-gling disease) and were confused with those of sarcoid-osis (7–10,14,22,24). In 1952 Komins proposed thatthese osseous lesions were a separate entity from lesionsof sarcoidosis. However, in recent series, solitary in-volvement appears to be the predominant skeletal mani-festation. Although vertebral and synovial involvementis well known, solitary osseous lesions of tuberculosis inchildren are uncommon. Few series have appeared in therecent literature describing these lesions (13,23,27,29).The majority have been case reports (1,2,5,7,12,15,21,31) or part of a large series of mainly adults(3,6,11,16–18,25,28,32). The variable clinical and radio-logic picture of isolated bone lesions in children maymimic subacute and chronic pyogenic osteomyelitis, fun-gal infections, cartilaginous tumors, simple and aneurys-

mal bone cysts, osteoid osteoma, eosinophilic granuloma,and Ewing sarcoma (1–3,7,11,13,16,17,22,24,28,29).

The lack of familiarity with the spectrum of bone le-sions may lead to delayed diagnosis. The purpose of thisreport is to describe the protean radiologic manifesta-tions of the osseous lesions of tuberculosis in sites otherthan the spine and synovium in the hope of stimulating ahigh index of suspicion for early diagnosis.

METHODS

We reviewed the clinical records and radiographs of42 children with osseous lesions of tuberculosis diag-nosed and treated at King Edward VIII Hospital, Durban,between 1984 and 1999. Lesions involving the spine andjoint synovium primarily were excluded. The clinical andradiologic features are listed in Table 1. There were 31boys and 11 girls with an age range of 1 to 12 years(average 6). Pain, swelling, and limp, when the lowerlimb was involved, were the main clinical features. Fourchildren had a fluctuant abscess (Fig. 1) and two othershad discharging sinuses. Six children had a history ofminor trauma. A family history of tuberculosis was re-corded in eight children. Symptoms ranged in durationfrom 3 weeks to 2 months. There were a total of 50lesions. Five children had multifocal bone involvement(patients 2, 3, 6, 24, and 34). The majority, 25 lesions,were in the metaphyses of long bone; 3 occurred in thediaphyses, 4 in the epiphyses, 8 in the short tubular bones(hands, feet), 7 in the flat bones (pelvis, clavicle), and 3in the small round bones (patella, talus, navicular).

Four basic patterns of bony lesions were seen: 26 ofthe cystic type, 10 infiltrative, 8 focal erosions, and 6spina ventosa lesions. Some lesions had a mixed pattern

Address correspondence and reprint requests to Dr. Mahomed NoorRasool, Department of Orthopaedics, Nelson R. Mandela School ofMedicine, Private Bag 7, Congella, 4013, Durban, South Africa(e-mail: [email protected]).

From the Department of Orthopaedic Surgery, Nelson R. MandelaSchool of Medicine, Durban, South Africa.

Journal of Pediatric Orthopaedics21:749–755 © 2001 Lippincott Williams & Wilkins, Inc., Philadelphia

749

but one radiologic type predominated. Soft tissue swell-ing and osteoporosis were seen in all radiographs. Mostof the lesions were of the cystic variety, located in themetaphysis, typically radiolucent, round to oval withslightmarginal sclerosis (Figs. 1–4,6).Somewereexpand-ing, others honeycombed and multiloculated. Cystic le-sions measured 0.5 to 3 cm in diameter. A periostealreaction was seen in three instances and a sequestrum infour. Four lesions crossed the growth plate. Infiltrativelesions resembled chronic osteomyelitis with slight peri-osteal reaction and diffuse bone destruction or perme-ation (Fig. 1). A pathologic fracture was seen in onepatient (patient 25). Six lesions crossed the growth plate.

Focal erosions were either localized areas of erosion andlysis with cortical breakdown or punched-out lesionswith slight marginal sclerosis (Fig. 5). Spina ventosalesions were typically expanding or fusiform, with denseperiosteal reaction. These lesions were seen in the meta-carpals (patient 34) and forearm bones (patients 32, 33)(Figs. 7, 8).

Plain radiographs of the affected area and chest wereobtained in all patients. Eight children had associatedchest involvement. Tomograms were obtained in fourpatients (patients 9, 15, 16, 18) (Fig. 3) and computedtomography scans in three (patients 9, 15, 18) to enablebetter definition and to plan biopsy of bony lesions.

TABLE 1. Characteristics and outcome of osseous lesions of tuberculosis

PatientAge,sex Anatomic sites Type Radiologic features

Follow-up(years) Outcome of healing

1 1F Proximal humeral metaphysis Cystic Unilocular 0.5 Complete2 1F Distal humeral metaphysis Cystic Multilocular, periostitis 3 Complete

Distal femoral metaphysis Cystic Unilocular Small distal humerusProximal tibial metaphysis Cystic Unilocular Complete

3 3M Distal humeral metaphysis Cystic Unilocular 3 CompleteProximal radial diaphysis Infiltrative Permeative Complete

4 1.5M Distal tibial metaphysis Cystic Multilocular 9 Complete5 1F Proximal ulna metaphysis Cystic Unilocular 9 Complete FFD 10°6 4M Thumb metacarpal Cystic Honeycombed 8 Short thumb metacarpal

Proximal phalanx finger Cystic Honeycombed Complete7 7M Distal tibial metaphysis Cystic Unilocular crossing physis 2 Complete8 9F Greater trochanter Cystic Unilocular 1 Slight sclerosis9 10M Talus Cystic Unilocular 1.5 Complete

10 1M Femoral neck Cystic Unilocular 1 Coxa vara, shortening 1 cm11 2M Femoral neck Cystic Unilocular 1.5 Slight sclerosis12 3M Femoral neck Cystic Unilocular 1 Complete13 2M Proximal tibia Cystic Unilocular 0.5 Complete14 1M Distal femoral metaphysis Cystic Unilocular crossing physis 1.5 Complete15 8M Distal femoral metaphysis Cystic Unilocular crossing physis 1.5 Complete16 3F Distal femoral metaphysis Cystic Unilocular crossing physis 1 Complete17 1F Proximal femoral epiphysis Cystic Unilocular 1 Complete18 9F Proximal femoral epiphysis Cystic Unilocular 1 AVN femoral head, FFD 20°19 8M Distal femoral epiphysis Cystic Unilocular, sequestrum 0.5 Slight sclerosis20 4F Proximal femoral metaphysis Cystic Several small cysts 5 Shortening 1.5 cm21 4M Metatarsal Cystic Unilocular, dense periostitis 2 Sclerosis22 3M Proximal tibial metaphysis Cystic Unilocular crossing physis 0.5 Complete23 5M Proximal tibial metaphysis Cystic Unilocular 2 Complete24 3M First metatarsal Infiltrative Destructive 1 Sclerosis

Navicular Infiltrative Destructive AVN navicular25 3M Clavicle Infiltrative Destructive, pathologic fracture 1 Slight sclerosis26 4M Clavicle Infiltrative Destructive 2 Slight sclerosis27 5M Clavicle Infiltrative Destructive 1.5 Complete28 6F Distal humerus Infiltrative Erosion olecranon fossa 2 Complete29 4M Femoral neck Infiltrative Destructive 1 Slight, sclerosis30 4M Femoral neck Infiltrative Destructive, periostitis 1 Sclerosis, shortening 1 cm31 1.5M Proximal femur Infiltrative Destruction into epiphysis 2 Shortening 2 cm, coxa vara32 1M Radial diaphysis Spina ventosa Fusiform, periostitis 1 Remodeled33 3M Ulna diaphysis Spina ventosa Fusiform, periostitis 1 Residual sclerosis

Remodeled34 4M Four metacarpals Spina ventosa Fusiform, dense periostitis 4 Remodeled, MPJ contracture,

metacarpal, carpal changes35 8F Clavicle (lateral end) Focal erosion Localized destruction 1.5 Complete36 6M Patella Focal erosion Punched out 1 Complete37 3M Radial epiphysis Focal erosion Punched out 0.5 Wrist stiffness38 2M Femoral neck Focal erosion Punched out 1 Slight sclerosis39 2M Femoral neck Focal erosion Localized destruction 2 AVN femoral head FFD 30°40 9F Pelvis, periacetabular Focal erosion Punched out 2 FFD 30°, ankylosis hip41 6M Pelvis, pubis Focal erosion Localized destruction 1.5 Sclerosis42 12M Pelvis, ilium Focal erosion Punched out 2 Complete

AVN, avascular necrosis; FFD, fixed flexion deformity; MPJ, metacarpophalangeal joint.

M. N. RASOOL750

J Pediatr Orthop, Vol. 21, No. 6, 2001

Technetium bone scans were obtained in all patients toexclude multifocal osseous lesions.

The erythrocyte sedimentation rate (ESR) was in-creased in 35 patients (range 33–108, average 61) andwas normal in 7 patients. A positive tuberculin skin testwas seen in 38 children; it was negative in 4. In sixchildren both the ESR and tuberculin skin test were nor-mal. HIV tests, obtained in patients with multifocal le-sions, were negative.

The hemoglobin level ranged between 8 and 13 g/L.The white cell counts were within normal limits. In allpatients the diagnosis was confirmed histologically. Carewas taken to obtain a biopsy sample from the osteolytic

lesion and not the adjacent joint synovium alone. Thelesion was curetted when a bone defect was found. Nobone graft was used to fill large defects. After surgery thelimb was immobilized in an appropriate plaster splint for3 to 4 weeks. Physiotherapy was commenced after re-moval of splint. Oral antituberculosis therapy was con-tinued for a year, using rifampicin, isoniazid, and pyra-zinamide.

RESULTS

The average follow-up was 2.5 years (range 0.5–9).Clinical and radiologic improvement was noted by 4 to 6weeks. Five patients were lost to follow-up after 6months. All lesions healed radiologically by 3 to 6months without relapse or recurrence (Figs. 2, 4, 7, 8).Slight sclerosis was seen radiologically in 12 patients.Cystic cavities healed completely with residual marginalsclerosis. Lesions crossing the growth plate healed com-pletely. Growth disturbance was seen in six patients, re-sulting in shortening in four lower limbs; a small thumbmetacarpal and small distal humerus were seen in theremaining two patients. Good remodeling of spina ven-tosa and expanded cystic lesions occurred in all in-stances. Evidence of avascular necrosis was seen in thefemoral head (three patients) and the navicular (one pa-tient). Coxa vara occurred in two hips.

DISCUSSION

Tuberculous osteomyelitis is less common than skel-etal tuberculosis involving the spine and synovial joints.In 50% of patients the vertebrae are the sites of skeletalinvolvement; the synovium is involved about 25%(11,30). Martini (17) in a large series of 652 cases ofbone and joint tuberculosis found bone involvement ofonly 11% in children.

The clinical and radiologic presentation of osseoustuberculosis appears to be changing. Destructive, dis-seminated, and multifocal lesions are less common thanthey were 50 years ago. Tuberculosis of bone was re-ported to be a predominantly destructive process that

FIG. 2. A: Radiographs of forearm in a 1-year-old (patient 5) showing a cystic lesion in the proximal ulna that is radiolucent, expanding,and round, with slight marginal sclerosis. B: Radiograph 8 years later shows healing after curettage and antituberculosis therapy.

FIG. 1. A–B: Lateral and anteroposterior radiographs of a3-year-old (patient 3) shows multifocal tuberculosis with a cysticlesion in the distal humerus and an infiltrative lesion in the proxi-mal radial diaphysis. There is a large abscess anteriorly.

OSSEOUS TUBERCULOSIS 751


occurs almost always secondary to a primary focus, andin 75% of patients the focus was found in the lungs (8).However, in recent reports, solitary, isolated bone lesionsappear to be the predominant radiologic type seen inchildren (1,2,5,13,16,17,21,23–25,27). Primary bone in-volvement is usually discovered late because symptomsare subtle. Diagnosis has been reported to be overlookedin favor of more commonly encountered lesions such aspyogenic osteomyelitis, fungal infection, osteoid os-teoma, and benign and malignant tumors (1–3,7,24,32).Some patients were reported to have been treated withnonsteroidal antiinflammatories for some of these benignconditions before the diagnosis of tuberculous osteomy-elitis was made (28).

In children the metaphyses of long bones, especially ofthe lower limbs, appear to be common sites of involve-ment, compared with the axial skeleton and pelvis inadults (30). Four basic types of bone lesions were seen inthis study: cystic, infiltrative, focal erosions, and spina

ventosa. The cystic form of bone tuberculosis is wellknown and has been the most common type reported inthe literature (7,14–17,27). Localization in various longbones and flat bones as single or multiple foci has beendescribed more commonly in children. Typically the cys-tic bone lesions are radiolucent, round to oval, and aresituated in the peripheral skeleton near the metaphysis(Figs. 1, 2). The cystlike appearance results from mar-ginal sclerosis. Martini (17) described the cystic lesionsas geode-like cavities. The cavity may contain a seques-trum of necrotic cancellous bone, described by Frenchauthors as image en grelot (grelot � little sphericalbells) (17). These “cysts” can mimic various benign tu-mors and granulomatous bone lesions (1–3,22,24). Infil-trative lesions (Fig. 1) are more diffuse areas of bonedestruction with permeation and little or no periostealreaction, resembling chronic pyogenic osteomyelitis,fungal infection, and Ewing sarcoma (28). Focal erosionsare small, localized areas of osteolysis (Fig. 5), usuallysituated eccentrically, with or without destruction of the

FIG. 3. Computed tomography scan of the body of the talusshowing a cystic lesion with marginal sclerosis (patient 9).

FIG. 4. A: Radiograph of the hip in a 4-year-old (patient 20) shows multiple small cysts in the femoral neck, osteoporosis, and slight jointspace widening. B: Radiograph 5 years later shows healing of the femoral neck with shortening.

FIG. 5. Radiograph of the knee in a 6-year-old (patient 36)shows focal erosion in the superior pole of the patella with os-teoporosis.

M. N. RASOOL752


cortex. Some lesions were punched-out defects with mar-ginal sclerosis; others were localized areas of destructionwith slight periosteal reaction but no marginal sclerosis.These lesions can resemble subacute pyogenic osteomy-elitis, eosinophilic granuloma, nonossifying fibroma, andneuroblastoma (1,2,11).

The expansile lesion (Figs. 7, 8) results from under-lying bone destruction with periosteal thickening, givingthe appearance termed spina ventosa (spina � shortbone, ventosa � filled with air) (28). A cystlike cavitymay form, and the bone shaft appears to be ballooned out

in a fusiform appearance. Sequestrum formation may oc-cur. Although more commonly seen in the short tubularbones of the hands and feet (1–3,5,16–18), similar le-sions can appear in the forearm bones and clavicle(1,28). Spina ventosa lesions were the least common typeseen in this and other series (17), and they remodeledwell after treatment.

Although four basic forms of bone changes were seenin this study, there was a combination of two or moretypes in some patients, with one type usually predomi-nating. Some authors have described other patterns ofbone lesions, but these have been mainly in adults (8,17,18,28).

Although it has been stated that tuberculosis of bone isalmost always secondary to a primary focus in the chest(8), no history of tuberculosis infection or exposure maybe present. Evidence of concurrent active intrathoracictuberculosis is present in <50% of patients (6,11,32).Similar to other reports (3,11,15), we found 20% withassociated chest involvement. Wang et al. (29) found noinstances of chest infection in their series of BCG osteo-myelitis.

Children with bone lesions usually present with localpain, swelling, tenderness, muscle wasting, and de-creased range of movement. Fluctuance, sinus discharge,and enlarged lymph nodes, which were alerting clinicalsigns in some series (15,17,20,28), were not common inthis study.

It has been suspected that trauma may play an impor-tant role in the pathogenesis of bone tuberculosis. Le-sions may remain dormant and asymptomatic and maybe revealed only after minor trauma (6,11,29). Minortrauma can mask the underlying pathology and cause adelay in diagnosis and treatment (29).

Impaired host resistance may also activate dormantlesions (11). Kumar and Saxena (15) proposed that bone

FIG. 6. Radiograph of the foot showing a small cyst in the firstmetatarsal with dense surrounding sclerosis and a central nidusresembling osteoid osteoma (patient 21).

FIG. 7. A: Radiograph of the forearm in a1-year-old (patient 32), showing a spina ventosalesion of the radius and expansion of the shaftwith periostitis and cystlike lucencies. B: Radio-graph at 1 year, showing healing and remodel-ing after curettage and antituberculosis treat-ment.



lesions were usually solitary because sensitization of thepatient to the tubercle bacillus occurred before the onsetof skeletal disease. However, if host immunity is poorand the immune response has been altered, the lesionsmay multiply. Several authors have reported a delay inthe diagnosis of bone tuberculosis (17,28,29). A normalESR and negative skin tests do not exclude a diagnosis oftuberculosis. Other authors have also recorded similarfindings in bone tuberculosis (17,28,29). The importanceof accurate diagnosis by bacteriologic and histologic in-vestigation has been emphasized in large reports (6,17,27,29). Versveld and Solomon (27) suggested that inbone lesions near a joint, the biopsy material should betaken from this area rather than the synovium alone,because the latter may show nonspecific changes. Curet-tage alone has been reported to yield favorable results(11,14,20,29). Bacilli sequestrated in necrotic tissue, es-pecially in cavities and bone defects, are inaccessible tochemotherapeutic agents. Therefore, curettage and de-bridement should be performed to exclude pyogenic andfungal infections, which are commonly seen in our en-vironment. Bone grafting of defects, as suggested bysome (15), was not performed in our series and others(16,17). Good resolution and remodeling of involvedbone was seen in this and other series (5,17,27).

According to Watts and Lifeso (30), there are no fea-tures pathognomonic of tuberculosis radiologically. Os-teopenia, soft tissue swelling, and minimal periosteal re-action may occur. Sequestrum formation is not common,and pathologic fractures are rare (30). Although meta-physeal lesions cross the physis, growth problems areuncommon after healing (27,30). A bone scan is helpfulin detecting other skeletal lesions (15,24).

BCG osteomyelitis, reported by several authors, canmanifest with radiologic features similar to those of tu-berculous osteomyelitis (4,19,29). The lesions are usu-ally localized to the epiphysis and metaphysis of long

bones, occasionally extending across the epiphyseal line.The interval between BCG vaccination and the onset ofsymptoms is usually a few months to 5 years. A confi-dent diagnosis requires growth of the BCG strain in cul-ture and a negative guinea pig test.

The diagnosis of musculoskeletal tuberculosis remainsa challenge to clinicians and requires a high index ofsuspicion. The lack of familiarity with the spectrum ofbone lesions can lead to delays in diagnosis. The destruc-tive changes of advanced tuberculosis are less commonlyencountered. Solitary lesions can mimic various benignbone lesions. Tuberculosis must be confirmed by histol-ogy or a positive culture.

Acknowledgment: The author thanks B. Katia for typingthis manuscript.

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Osseous Manifestations of Tuberculosis in Children.9