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Primary Pyomyositis
J. Bickels, L. Ben-Sira, A. Kessler and S. Wientroub J Bone Joint Surg Am. 2002;84:2277-2286.

This information is current as of July 4, 2007 Supplementary material Commentary and Perspective, data tables, additional images, video clips and/or translated abstracts are available for this article. This information can be accessed at http://www.ejbjs.org/cgi/content/full/84/12/2277/DC1 Click here to order reprints or request permission to use material from this article, or locate the article citation on jbjs.org and click on the [Reprints and Permissions] link. The Journal of Bone and Joint Surgery 20 Pickering Street, Needham, MA 02492-3157 www.jbjs.org

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COPYRIGHT © 2002
BY

THE JOURNAL

OF

BONE

AND JOINT

SURGERY, INCORPORATED

Current Concepts Review

Primary Pyomyositis
BY J. BICKELS, MD, L. BEN-SIRA, MD, A. KESSLER, MD, AND S. WIENTROUB, MD
Investigation performed at the Departments of Pediatric Orthopaedics and Radiology, Dana Children’s Hospital, Tel-Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel
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Primary pyomyositis is a rare, subacute, primary muscle infection that is probably the result of a transient bacteremia in most patients. The quadriceps, gluteal, and iliopsoas muscles are the most commonly affected anatomic sites. Staphylococcus aureus is the culpable bacteria in >75% of cases. There are three consecutive stages of the disease: diffuse muscle infection, abscess formation, and sepsis. Magnetic resonance imaging is the preferred diagnostic imaging modality. Treatment includes complete drainage of any abscess cavity combined with appropriate antibiotic therapy. Drainage is performed either by open surgical exposure or by needle aspiration guided by computerized tomography or ultrasonography. Most patients have complete recovery with no long-term sequelae.

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Primary pyomyositis (also called tropical myositis, infective myositis, pyogenic myositis, suppurative myositis, myositis purulenta tropica, epidemic abscess, or bacterial myositis) is a subacute, deep bacterial infection of skeletal muscle. It is not secondary to a contiguous infection of the skin, bone, or soft tissues1-8. It commonly manifests as a local abscess but may also present as a diffuse inflammatory or a rapidly progressing myonecrotic process8-11. While pyomyositis is frequently seen in many parts of Africa and the South Pacific, it is rare in the United States and other temperate climates4-7. Because of its rarity and often vague clinical presentation, it is unlikely to be considered during the initial diagnosis. Moreover, the diagnosis may be delayed if the affected muscle is deeply situated and local signs are not apparent. This delay in diagnosis may result in a compartment syndrome, extension into and destruction of an adjacent joint, sepsis, and occasionally death. Lung and brain abscesses, pericarditis, myocarditis, endocarditis, and renal failure have also been reported8,12-20. The long-term sequelae of pyomyositis include osteomyelitis of adjacent bones, muscle-scarring, residual weakness, and functional impairment17,21-23. Drainage of the muscle abscess followed by administration of appropriate antibiotics remains the mainstay of treatment and usually leads to complete recovery21,24. Most reports of primary pyomyositis have been either case reports or reports of small series of patients1,2,5-7,10-18,20,22-103, and it is difficult to formulate a generalized concept of diagnosis and treatment from such sources. The present article summarizes the results and findings in 676 patients with primary

pyomyositis reported in the English-language literature from the early 1960s to date. We review the epidemiology, pathophysiology, and clinical presentation of the disease and guidelines for patient management. Epidemiology Primary pyomyositis has been seen in all age-groups, but it is most common in the first and second decades of life and there is a slight male predominance1,4,21,31,60,69,87,104. In our review, the ages of the patients ranged from two months to eighty-two years, with a mean of 28.1 years (Fig. 1). Primary pyomyositis can involve any muscle group in the body: a single muscle is usually affected, although 11% to 43% of patients have involvement of multiple sites4,8,15,19,29. Our review of the cases of 676 patients identified 112 (16.6%) with multiple-site involvement. One of the largest studies of primary pyomyositis was performed by Chiedozi, who reported on 112 patients seen in Nigeria over a period of four years4. The most common site of infection was the quadriceps muscle, followed by the gluteal and iliopsoas muscles4. This observation was confirmed by others3,4,14,21-23,44,104-107, who noted that pyomyositis usually involves the largest muscle groups located around the pelvic girdle and lower extremities. Figures 2-A and 2-B summarize the anatomic distribution of primary pyomyositis in the 676 patients included in our review1-7,9-30,32-38,40-51,53-92,94-107. Iliopsoas pyomyositis was long considered to be the most common form of this infection. However, most of these cases were actually secondary infections that had developed as an ex-

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Fig. 1

Age distribution of the patients with primary pyomyositis in our review.

tension from adjacent tuberculosis in the spine or iliac lymph nodes39,65. Indeed, prior to modern antituberculous therapy, iliopsoas pyomyositis developed in up to 20% of patients with spinal tuberculosis and, conversely, the diagnosis of an iliopsoas abscess was most likely associated with tuberculosis. Today, secondary iliopsoas pyomyositis is most commonly associated with gastrointestinal or urinary tract infection23,46,52,103. In these cases, muscle infection and subsequent abscess formation are probably the result of direct extension of the adjacent infection23. Primary iliopsoas pyomyositis is rare, and the diagnosis is usually delayed because of the deep location of the muscle and because symptoms often resemble those of a primary infection in the hip31. In 1966, Lam and Hodgson described in detail the cases of twenty-four patients who presented with a primary psoas abscess106. Because the authors were unable to detect spinal involvement in these patients, they called this entity “nonspinal pyogenic psoas abscess.”106 Malhotra et al. reported on forty-one patients with a psoas abscess who had been seen over a period of fourteen years60. Only fourteen of those patients had primary pyomyositis; the remaining twenty-seven had pyomyositis secondary to spinal tuberculosis. The bacteria causing the infection frequently are not isolated from blood cultures or cultures of purulent material. Of 452 patients with primary pyomyositis in whom the culpable bacteria were identified1,2,4-19,21-104,106-108, 77% (350) had a positive culture for Staphylococcus aureus. Other isolates included Streptococci, Escherichia coli, Salmonella enteritidus, and Mycobacterium tuberculosis (Table I). Pathophysiology The etiology of primary pyomyositis remains unclear. The infection is believed to be a complication of transient bacteremia because, in the vast majority of patients, it develops without an obvious penetrating injury or any other clear portal of entry4,10,30,60,108. The rarity of the infection is attributed to an assumed resistance of skeletal muscles to bacteremic episodes. Intravenous injection of sublethal doses of Staphylococcus aureus did not produce pyomyositis in animals until the muscles were traumatized by pinching, electric shock, or ischemia31. These findings are compatible with those of Smith

and Vickers, who reported only two muscle abscesses in 327 patients who had died of staphylococcal septicemia109. They suggested that bacteremia alone is not sufficient to cause an intramuscular abscess; a concomitant muscle abnormality is required. Trauma to the affected muscle resulting in alteration of the muscle structure has been proposed as a possible etiology2,69. It has been hypothesized that trauma alters local muscle tissue structure, thereby creating a locus minoris for implantation of bacteria from a subsequent, unrelated bacteremic episode88. This could also explain the appearance of pyomyositis after forceful muscle contractions due to epileptic seizures or electric shock72. When patients with primary pyomyositis have a history of trauma, it usually involved a direct blow to or near the involved muscle44, with the pyomyositis appearing from days to a few weeks after the injury10. Clinical reports, however, have not provided evidence supporting this theory because, although trauma to the lower extremities is extremely common, pyomyositis is rare. Moreover, the reported prevalences of confirmed trauma to the affected site in patients with primary pyomyositis are conflicting, with percentages ranging from <7% to 39%4,21,44,60,77,107. A history of trauma was reported in <5% of the 676 patients in the current review. Jackson and Feagin reported that, of 250 young athletes who sustained a contusion to the quadriceps muscle, not a single one had pyomyositis; instead, myositis ossificans developed in some individuals, all of whom had moderate-to-severe injury110. Muscle tissue structure may also be altered by a subclinical infection caused by parasites or viruses. The high prevalence of primary pyomyositis in the tropics has led some researchers to speculate that microscopic foci of necrotic muscle that are at risk for bacterial seeding develop in patients who have a migrating parasitic infection1,5,8,105,111. However, the geographic distribution of pyomyositis does not match that of parasitic infection4. Furthermore, many patients from tropical countries who present with pyomyositis are entirely free of active parasitic infection4. A preceding viral infection is occasionally documented. Taylor et al. performed ultrastructural studies on apparently normal muscles in patients with tropical myositis and documented intracellular particles and a lymphocytic infiltrate

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nous drug abuse4,11,24,31,40-42,49,55,56,63,71,78,84,96,101,107. Christin and Sarosi found that, of ninetyfive patients with pyomyositis, 17% had HIV infection and 5% had hematologic malignant disease31. A review of the literature suggests that approximately half of patients presenting with pyomyositis when they are more than thirty years of age have an underlying condition. Pyomyositis has also been associated with thiamine deficiency, scurvy, and beriberi31,113. Since vitamin deficiencies and nutritional parameters are rarely mentioned in North American reports, their role in predisposing patients to the infection remains uncertain. Clinical Manifestations The microbiologic profile and clinical manifestations of pyomyositis in the United States and Europe are indistinguishable from those reported (with far

Fig. 2-A

Figs. 2-A and 2-B Anatomic distribution of the infections in the 676 patients with primary pyomyositis in our review.

consistent with a primary viral etiology in two of nine specimens112. A similar association was reported by Dow et al., who described a twenty-six-year-old patient with hepatitis-A infection and concomitant bilateral pain in the thigh; pyomyositis developed in one thigh a few weeks later36. Patients with pyomyositis who are older than thirty years of age commonly have an underlying disease or condition that might impair the immune system. These conditions include diabetes mellitus, malnutrition, HIV (human immunodeficiency virus) infection or AIDS (acquired immunodeficiency syndrome), malignant tumors, autoimmune and chronic liver diseases, and intrave-

Fig. 2-B

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TABLE I Infectious Agents Causing Primary Pyomyositis, Isolated from Four Hundred and Fifty-two Patients with Confirmed Primary Pyomyositis1,2,4-19,21-104,106-108 Infectious Agent Staphylococci Staphylococcus aureus Staphylococcus epidermidis Streptococci β-hemolytic group-A Streptococcus β-hemolytic group-G Streptococcus Group-B hemolytic Streptococcus Group-C Streptococcus Group-D Streptococcus Non-group-A B Streptococcus Anaerobic Streptococcus Streptococcus pyogenes Streptococcus viridans Streptococcus pneumoniae Streptococcus faecalis Streptococcus anginosus-constellatus Streptococci; not further specified Mixed staphylococcal-streptococcal infection Gram-positive cocci; not further specified Escherichia coli Salmonella enteritidis Mycobacterium tuberculosis Clostridium septicum Prevotella melaninogenica Candida albicans Aeromonas hydrophila Citrobacter freundii Fusobacterium nucleatum Haemophilus influenzae Klebsiella pneumoniae Klebsiella oxytoca Neisseria gonorrhoeae Pseudomonas enterics yeast Yersinia enterocolitica Enterococcus Proteus Total No. of Patients 350 2 19 1 4 1 1 1 1 11 3 4 1 1 7 2 3 11 7 5 2 2 2 1 1 1 1 1 1 1 1 1 1 1 452

greater frequency) in the tropics1,4,21,31,87,104,108. Pyomyositis typically has a subacute clinical course, and patients first seek medical assistance at an average of five to six days after the onset of signs and symptoms. Children may have a more acute presentation, whereas patients with immunosuppression may have a more prolonged course of up to a few weeks21,77,87,94,104.

Primary pyomyositis has three distinct stages, which represent a gradual progression from diffuse inflammation to focal abscess formation to a septic state4,7,12,26,29,32,41,44,58,60,64,66,76,79,86,87,92,102,107,108. Stage 1: Primary pyomyositis typically begins with the insidious onset of dull, cramping, progressive pain associated with a low-grade fever, general malaise, and muscle ache. Sealed by the muscle aponeurosis and deep fascia, an inflammatory process within a muscle does not reach the subcutaneous tissues and overlying epidermis in the early course of the infection. As a result, there is a short period during which local signs of inflammation are absent but pain and even systemic signs of infection are present. Thus, the more common etiologies of fever and musculoskeletal pain are initially considered, and one to two weeks may elapse before the correct diagnosis is made and appropriate treatment can be instituted. Stage 2: Muscle abscess formation, the stage during which most patients are first seen, is associated with local and systemic manifestations of infection. A tender soft-tissue mass can be palpated, and the affected muscle is typically described as having a firm, wooden texture. The overlying skin is swollen, erythematous, and warm. The patient may have exquisite tenderness and fluctuance of the involved area, obvious functional disability, and occasionally frank septicemia. Although it is rare, streptococcal pyomyositis can take the form of a rapidly progressing, diffuse muscle necrosis rather than local abscess formation because of the inherent aggresssiveness of those bacteria. For this reason, patients with streptococcal pyomyositis tend to present with a fulminating course of intense pain, high fever, and diffuse swelling and erythema. Stage 3: If pyomyositis is not treated in the second stage, it may progress to the third stage, which includes signs of toxicity and septic shock. This late stage of the disease is characterized by severe pain, local signs of infection, and systemic manifestations of sepsis, all of which require urgent intervention. Because of its clinical manifestations, pyomyositis has been confused with muscle strain, thrombophlebitis, cellulitis, bursitis, contusion, hematoma, Perthes disease, septic arthritis, osteomyelitis, rheumatoid disease, and soft-tissue sarcoma14,25,30,35,72,73,76,79,92,107. Pyomyositis of the iliopsoas or involvement of the abdominal wall, especially the right lower quadrant, may be confused with acute appendicitis and lead to unnecessary laparotomy14,99,104. A comprehensive medical history, meticulous physical examination, and judicious use of imaging studies can establish the diagnosis in the majority of patients. Pyomyositis of the iliopsoas muscle produces a distinct clinical syndrome. Clinical findings are often insidious in presentation and reflect the retroperitoneal location of the muscle and its proximity to intra-abdominal structures, the femoral nerve, and the hip joint69,72. Presenting symptoms include deep, diffuse pain in the back, flank, or hip. The patient may walk with a limp or refuse to move the hip, and the affected thigh is often held in flexion and external rotation25,30,72. Simple movements that stretch the iliopsoas muscle group, such as extension or internal rotation of the affected hip, may also

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Fig. 3

Contrast-enhanced computerized tomography scan of a sixty-seven-year-old woman with pyomyositis of the right psoas muscle, showing asymmetric enlargement of the muscle with abscess formation (arrows). I = iliacus muscle, P = psoas muscle. (Figure kindly provided by Dr. R. Zissin.)

elicit pain. There may be hyperlordosis and scoliosis toward the affected side. Physical examination usually reveals a tender mass in the flank or just above the inguinal ligament, and this is more effectively assessed with a rectal examination. Abdominal guarding or rigidity may not be prominent60,83. Before the advent of computerized tomography, iliopsoas pyomyositis was described infrequently. Because its onset is insidious and its signs and symptoms are obscure, its diagnosis and treatment were usually delayed and, not uncommonly, awaited exploratory laparotomy to identify the specific focus and to implement operative drainage107. The emergence of HIV infection and AIDS has been accompanied by an increase in the number of reported cases of

pyomyositis. Patients with these conditions may have an increased risk of multifocal disease, an atypical presentation (e.g., progressive weakness and myalgia), and minimal symptoms because of neutrophil dysfunction24,31,80,94,98,107. Thus, the diagnosis of pyomyositis should be considered and appropriate evaluations should be performed promptly for any patient with HIV infection who complains of a painful, swollen muscle80,84. A similar phenomenon has been observed in patients with tuberculous pyomyositis, who may present with symptoms of a few months’ duration associated with minimal elevations of the white blood-cell count and the erythrocyte sedimentation rate54. Routine laboratory evaluation is rarely helpful in the

Fig. 4-A

Figs. 4-A, 4-B, and 4-C An eleven-year-old boy with pyomyositis of the right iliopsoas muscle following trauma to the hip. Fig. 4-A Ultrasonogram demonstrating hypoechoic enlargement of the muscle with internal debris, typical of local abscess formation (arrows).

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Fig. 4-B

The contralateral normal iliopsoas muscle is shown (arrows).

diagnosis of pyomyositis, as recognition of this condition is based on the clinical presentation and the results of imaging studies. Leukocytosis with a left shift and an elevated sedimentation rate are common4,25,31,33,42,60,77,87,114. Eosinophilia was reported in association with pyomyositis in the tropics, an observation that led to the hypothesis that these patients had an underlying parasitic infection4. However, eosinophilia has been rarely reported in North American patients with pyomyositis87. Serum levels of muscle enzymes are generally normal60,107,114. A review of the findings in 144 patients reported on in eight studies showed that cultures of blood and of purulent material are positive for only 16% to 38% and 21% to 41% of the patients, respectively10,21,22,87,92,106,107,114.

Imaging Studies Plain radiography is the appropriate study for the initial screening. However, only a minority of patients have findings suggestive of muscle inflammation or abscess formation on plain radiographs21,85. These findings, when present, include enlargement and loss of definition of the affected muscle, gas shadows in the soft tissues, and occasionally reactive changes in the adjacent bone60,87. The main role of plain radiographs is to rule out primary bone lesions, such as subacute osteomyelitis or primary bone sarcoma, that can mimic the clinical presentation of primary pyomyositis. Computerized tomography provides better delineation of muscle structure than does plain radiography and therefore

Fig. 4-C

Ultrasonography-guided needle aspiration (the arrows point to the needle within the abscess cavity) and intravenous administration of antibiotics were followed by rapid resolution of fever, pain, and local signs of infection.

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Fig. 5-A

Figs. 5-A and 5-B A four-year-old girl with fever, nonspecific hip pain, and a broad-based gait. Fig. 5-A Coronal inversion recovery magnetic resonance image revealing abnormal signal intensity limited to the left adductors (arrow).

enables the diagnosis of a muscle abscess. The typical finding on computerized tomography images is asymmetric enlargement of the muscle belly associated with a focal area of low attenuation or gas formation as well as peripheral enhancement after injection of contrast medium (Fig. 3)11,44,60,67,103,107. Computerized tomography may, however, fail to demonstrate diffuse inflammatory changes in the early stages of the infection. The fact that children often have little body fat may further decrease the contrast between soft-tissue structures, thus reducing the accuracy of this imaging modality. Ultrasonography has also been used for the diagnosis of pyomyositis. The typical findings on ultrasonographic imaging are a bulky muscle with abnormal echotexture and a hypoechoic focal lesion, occasionally with internal debris and air bubbles20,60,96 (Figs. 4-A and 4-B). Both computerized tomogra-

phy and ultrasonography enable guided percutaneous needle aspiration and drainage (Fig. 4-C)70,100,103. Magnetic resonance imaging is the most useful imaging modality for the diagnosis of pyomyositis as it most clearly demonstrates diffuse muscle inflammation as well as any subsequent abscess formation (Figs. 5-A and 5-B)69,101,115. The findings include diffuse muscle enlargement associated with an increase in signal intensity on T2-weighted images. The detection of an abscess is facilitated by the use of gadolinium enhancement68,69,77,91. Magnetic resonance imaging reveals osseous changes in the majority of patients, but these alterations probably represent the response to the adjacent inflammatory process rather than true osteomyelitis69,87. Moreover, magnetic resonance imaging allows exclusion of other pathological processes, such as infectious arthritis of the hip, osteomyelitis of the proximal part of the femur or the pelvis, hematoma, or soft-tissue tumor54,68,77. Although it is rarely used in the diagnosis of pyomyositis, technetium scintigraphy typically shows increased softtissue uptake at the blood-flow and pool phases. Delayed images, however, usually fail to show increased uptake in the adjacent bones57,87. Increased uptake at that phase suggests a prolonged course of the disease87. Gallium scintigraphy has also been used in the evaluation of pyomyositis. It may assist in the diagnosis when the clinical presentation is equivocal, and it may also detect additional foci of muscle abscesses that are suspected in patients who do not respond to drainage and antibiotic therapy45,52,57,75,107. Multifocal pyomyositis is relatively rare. When it occurs, a comprehensive medical history, meticulous physical examination, and judicious use of imaging studies will establish the diagnosis and detect the foci of infection. Treatment The choice of treatment for pyomyositis depends on its stage at presentation. During the early stage of the infection, the diffuse inflammatory changes can be effectively treated with antibiotics alone69,87. Abscess formation, however, requires appropriate drainage prior to the initiation of antibiotic therapy. Because most patients who have pyomyositis are not seen until after an intramuscular abscess has already formed, drainage followed by

Fig. 5-B

Axial T1-weighted image with fat saturation following injection of contrast medium, demonstrating diffuse muscle enhancement (arrow) with no evidence of abscess formation.

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intravenous administration of antibiotics remains the treatment of choice. Such treatment results in complete recovery with no long-term sequelae in the vast majority of cases21,22,24,25,44,60,92. However, osteomyelitis of adjacent bones, muscle-scarring, residual weakness, functional impairment, and a depression at the site of the infection indicating a defect in the underlying softtissues and muscle fibers have been reported17,21-23. Traditionally, abscesses had been drained by operative means, which entailed a large skin incision and wide exposure of the affected muscle. Similarly, iliopsoas pyomyositis necessitated laparotomy and extensive retroperitoneal exposure. Following operative drainage, application of packing and daily dressing changes were necessary to prevent the abscess cavity from closing prematurely104. Today, the use of large suction drains has replaced this method. These drains allow primary closure of the operative wound with continuous and adequate drainage of the abscess cavity. Drainage can now be accomplished percutaneously under ultrasonographic or computerized tomographic guidance, and operative intervention is used only when complete drainage cannot be achieved percutaneously or when such treatment is not available65,87,103. Streptococcal pyomyositis is associated with extensive muscle necrosis that requires not only abscess drainage but also radical excision of all necrotic tissue. When there has been a delay in diagnosis, a more extensive débridement and, rarely, amputation may be needed, whereupon recovery may be prolonged and possibly complicated17,66,74. In order to avoid interference with the microbiologic evaluation, antibiotic therapy is ordinarily given to the patient immediately following drainage of the purulent material. However, patients presenting in a septic state cannot afford this delay and require immediate administration of antibiotic therapy. Most patients with primary pyomyositis can be treated successfully with intravenous administration of a single antibiotic. On the basis of the most likely culpable bacteria, cloxacillin is a suitable and common choice5,45,57,63,68,69,77,87,104. Administration of a combination of cloxacillin and an aminoglycoside achieves a synergistic effect and is reserved for patients who are either in a septic state or immunocompromised49,77,116-118. There should be a major clinical improvement after drainage and the initation of intravenous antibiotics, and if the patient does not respond quickly to these measures the possibility that the drainage of the abscess was incomplete or that the patient has multifocal disease should be considered. Recommendations regarding the optimal duration and route of the medication reflect the wide range of differences in

the stages of the disease and the overall clinical status of the patient at presentation. Intravenous antibiotics are usually given first for a period of seven to ten days; the overall duration of this treatment should be proportional to the size of the lesion and the clinical status of the individual patient. Oral antibiotics, usually a first-generation cephalosporin, are then given for a total of five to six weeks7,10,28,60,83,87,114. Patients who have an underlying disease that compromises their immunity may require a longer period of intravenous and oral antibiotic treatment. Overview Primary pyomyositis is a rare clinical entity. The etiology is obscure in most cases, but the infection is believed to be a complication of transient bacteremia. Usually located around the large muscles of the pelvic girdle and lower extremities, it is often confused with the more common febrile diseases that are ubiquitous at these sites. Early diagnosis of pyomyositis is, therefore, challenging; careful attention to the medical history, a meticulous physical examination, and judicious use of imaging studies are essential for diagnosis and initiation of definitive treatment. Magnetic resonance imaging is the modality of choice for the diagnosis of pyomyositis, as it clearly defines the anatomic extent of the infection and differentiates between the early stage of diffuse muscle inflammation and the subsequent abscess formation. Computerized tomography and ultrasonography can clearly demonstrate an already formed muscle abscess and can guide percutaneous needle drainage. Early diagnosis, complete drainage of the purulent material, and use of appropriate antibiotic therapy are the key determinants of successful treatment and lead to complete resolution in the vast majority of these patients.

J. Bickels, MD L. Ben-Sira, MD A. Kessler, MD S. Wientroub, MD Departments of Pediatric Orthopaedics (J.B. and S.W.) and Radiology (L.B.-S. and A.K.), Dana Children’s Hospital, Tel-Aviv Sourasky Medical Center, 6 Weizman Street, Tel-Aviv 64239, Israel. E-mail address for S. Wientroub: pedorth@tasmc.health.gov.il The authors did not receive grants or outside funding in support of their research or preparation of this manuscript. They did not receive payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

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