Shoulder sepsis can have a devastating impact on shoulder function, particularly if diagnosis and treatment are delayed or inadequate. The general principles in the pathogenesis of shoulder sepsis are similar to those pertaining to all intra-articular infections. There are three fundamental pathways for pathogens to enter a joint:
- 1.
Spontaneous hematogenous seeding via the synovial blood supply
- 2.
Contiguous spread from adjacent metaphyseal osteomyelitis via the intra-articular portion of the metaphysis
- 3.
Penetration of the joint by trauma, therapy, or surgery ( Fig. 11-1 )
FIGURE 11-1
Sinus communicating with a prosthetic shoulder joint. This patient developed a chronic low-grade infection after undergoing a total shoulder arthroplasty.
Certain patient groups with immune system depression or aberrations are at increased risk for infection. Patients with rheumatoid disease can manifest a spontaneous and somewhat cryptic sepsis in joints. Diabetics, infants, children, older people, patients with vascular disease, drug abusers, and patients with human immunodeficiency virus infection have an increased susceptibility to specific organisms, as have patients with hematologic dyscrasias or neoplastic disease.
Joint infection requires a threshold inoculum of bacteria and can be facilitated by damaged tissue, foreign body substrata, and the acellularity of cartilage surfaces. Total joint arthroplasties are at potential risk of infection because of the presence of metal and polymer biomaterials and the decreased phagocytic ability of macrophages in the presence of methylmethacrylate. Biomaterials and adjacent damaged tissues and substrates are readily colonized by bacteria in a polysaccharide biofilm that is resistant to macrophage attack and antibiotic penetration. With antibiotic prophylaxis, infection rates of total joint arthroplasty have been reported to be low: 1% to 5%, depending on the device and the location. However, once infected, biomaterials and damaged tissues are exceedingly resistant to treatment.
Clinical infection in immunosuppressed patients involves the maturation of an inoculum of known pathogens (e.g., Staphylococcus aureus or Pseudomonas aeruginosa ) or the transformation of nonpathogens (e.g., Staphylococcus epidermidis ) to a septic focus of adhesive virulent organisms. This transformation can occur in the presence of, and be potentiated by, the surface of biomaterials, damaged tissue, and defenseless cartilage matrix surfaces.
History
Experiences in shoulder infection have paralleled those of other large joints, although with less frequency. The work of outstanding scientists, such as Louis Pasteur (1822-1895), Joseph Lister (1827-1912), and Robert Koch (1843-1910), in the last quarter of the nineteenth century ushered in the modern age of bacteriology and an early understanding of intra-articular sepsis. Koch’s experiments with culture media at the Berlin Institute for Infectious Disease verified the role of the tubercle bacillus in musculoskeletal infection.
The latter part of the nineteenth century also saw the development of the concept of antisepsis. Lister maintained that sepsis was the main obstacle to significant advances in surgery. He documented a dramatic reduction in cases of empyema, erysipelas, hospital gangrene, and surgical infection through the use of antiseptic techniques. Although the popularization of antiseptic techniques in the surgical theater greatly reduced the rate of complications resulting from infection, it was not until the 1930s that specific antimicrobial therapy was discovered. In 1935 a German bacteriologist, Gerhard Domagk, discovered that sulfonamides protected mice against fatal doses of hemolytic staphylococci. Sulfonamides were soon employed for infections in patients, with excellent results.
Although the history of bacteriology, antiseptic techniques in surgery, and the development of antibiotics are well documented, very little of the early literature relates specifically to infections about the shoulder. In Codman’s book, The Shoulder , first published in 1934, infections of the shoulder and, in particular, osteomyelitis of the proximal humerus were considered to be very rare lesions. Codman cited a report by King and Holmes in 1927 in which a review of 450 consecutive symptomatic shoulders evaluated at the Massachusetts General Hospital revealed five cases of tuberculosis of the shoulder, one luetic infection of the shoulder, three unspecified shoulder infections, and two cases of osteomyelitis of the proximal humerus. The rarity of tubercular lesions of the shoulder was documented through the results of four large series of tuberculosis involving the musculoskeletal system (Townsend, 21 of 3244 cases; Whitman, 38 of 1833 cases; Young, 7 of 5680 cases; and Billroth, 14 of 1900 cases). As microbial culturing and identification techniques developed in the early twentieth century, streptococcal and staphylococcal species were more often identified as the causative agents in shoulder infection.
Septic Anatomy of the Shoulder
A review of shoulder anatomy reveals specific structural relationships that are intimately linked to the pathogenesis of joint sepsis and osteomyelitis. The circulation of the proximal humerus and periarticular structures (particularly the synovium) and the intricate system of bursae about the shoulder are critical factors.
Classically, the age-dependent presentations of hematogenous osteomyelitis and septic arthritis of the shoulder (and of other large joints, such as the hip and knee) have been attributed to vascular development about the growth plate and epiphysis. The most detailed studies of the vascular development in this area have involved the proximal femur; however, this is analogous to the same development about the proximal humerus. Experimental work by Trueta demonstrated that before 8 months of age, there are direct vascular communications across the growth plate between the nutrient artery system and the epiphyseal ossicle. This observation was believed to account for the frequency of infection involving the epiphyseal ossicle and subsequent joint sepsis in infants. At some point between 8 and 18 months of age (an average of 1 year), the growth plate forms a complete barrier to direct vascular communication between the metaphysis and epiphysis. The last vestiges of the nutrient artery turn down acutely at the growth plate and reach sinusoidal veins. At this point the blood flow slows down, creating an ideal medium for the proliferation of pathogenic bacteria.
In the adult shoulder, the intra-articular extent of the metaphysis is located in the inferior sulcus and is intracapsular for approximately 10 to 12 mm. An infection of the proximal metaphysis, once established, can gain access to the shoulder joint via the haversian and Volkmann canals at the nonperiosteal zone ( Fig. 11-2 ). With the obliteration of the growth plate at skeletal maturity, anastomoses of the metaphyseal and epiphyseal circulation are again established.
In his study of the vascular development of the proximal femur in fetuses and children up to 14 years and 8 months, Chung found no evidence of direct communications between the metaphyseal and epiphyseal circulation across the growth plate in any age group. Chung’s work demonstrated a persistent extraosseous anastomosis between the metaphyseal and epiphyseal circulation on the surface of the perichondrial ring. He found no evidence of vessels penetrating the growth plate in the infant population and attributed apparent changes in the arterial supply with age to enlargement of the neck and ossification center.
Branches of the suprascapular artery and the circumflex scapular branch of the subscapular artery from the scapular side of the shoulder anastomose with the anterior and posterior humeral circumflex arteries from the humeral side of the shoulder. This anastomotic system supplies the proximal humerus by forming an extra-articular and extracapsular arterial ring. Vessels from this ring traverse the capsule and form an intra-articular synovial ring. This fine anastomosis of vessels in the synovial membrane is located at the junction of the synovium and the articular cartilage. This subsynovial ring of vessels was first described by William Hunter in 1743 and named the circulus articuli vasculosus. At the transitional zone, synovial cells become flattened over this periarticular vascular fringe. Fine arterioles at this boundary acutely loop back toward the periphery. Again, blood flow at this level can decrease, which provides a site for establishing an inoculum of pathogenic organisms. Rather than hemodynamic changes, however, it is more probable that receptor-specific, microbe-to-cell surface interactions potentiate the infectious process.
Another anatomic consideration in sepsis of the shoulder is the communication between the joint space and capsule and the system of bursae about the shoulder. Anteriorly, there is direct communication between the capsule and the subscapular bursa located just below the coracoid process. Posteriorly, the capsule communicates with the infraspinatus bursa. There is a third opening in the capsule at the point at which the tendon of the long head of the biceps enters the shoulder. From the transverse humeral ligament to its entry into the shoulder capsule, the tendon of the long head of the biceps is enveloped in folds of synovium. Intentional or inadvertent injection of the subscapular bursa, the infraspinatus bursa, or the tendon of the long head of the biceps provides the potential for intra-articular bacterial inoculation. Injection of the subacromial or subdeltoid bursa in the presence of a rotator cuff tear (degenerative or traumatic) provides further potential for bacterial contamination of the joint.
Ward and Eckardt reported on four patients with subacromial or subdeltoid bursa abscesses. Three of these four patients were chronically ill and debilitated, the bursal abscesses coexisting with clinically diagnosed mild to resolving glenohumeral pyarthrosis. The symptoms and signs of the abscesses were minimal in all four patients. The authors found that computed tomography (CT) or magnetic resonance imaging (MRI) can help to detect abscesses and plan treatment.
Microanatomy and Cell Biology
The hyaline cartilage of the articular surface is essentially acellular and consists of horizontally arranged collagen fibers in proteoglycan macromolecules. The boundaries of the joint cavity are composed of a richly vascularized cellular synovial tissue. It has been suggested that collagen fibers and the glycoprotein matrix, rather than the synovium, are the target substrata for microbial adhesion and colonization.
Some synovial cells are phagocytic and appear to combat infection as part of the inflammatory response. Microscopic examination of infected joints in a lupine animal model indicated predominant colonization of cartilaginous, rather than synovial, surfaces. Receptors for collagen have been identified on the cell surfaces of certain strains of S. aureus . The infrequent occurrence of bacteria on synovial tissue might reflect the innate resistance of synovial cells to colonization, the lack of appropriate synovial ligands, or functional host defense mechanisms at a synovial level. The subintimal vascularized layer contains fibroadipose tissue, lymphatic vessels, and nerves. Ultrastructural studies of the synovial subintimal vessels have revealed that gaps between endothelial cells are bridged by a fine membrane. There is no epithelial tissue in the synovial lining and, therefore, no structural barrier (basement membrane) to prevent the spread of infection from synovial blood vessels to the joint. The synovial lining in the transition zone is rarely more than three or four cell layers thick, placing the synovial blood vessels in a superficial position. Intra-articular hemorrhage caused by trauma, combined with transient bacteremia, may be implicated as a factor in the pathogenesis of joint sepsis. Hematogenous seeding can allow bacterial penetration of synovial vessels, producing an effusion consisting primarily of neutrophils that release cartilage-destroying lysosomal enzymes.
Articular (hyaline) cartilage varies from 2 to 4 mm in thickness in the large joints of adults. This avascular, aneural tissue consists of a relatively small number of cells and chondrocytes and an abundant extracellular matrix. The extracellular matrix contains collagen and a ground substance composed of carbohydrate and noncollagenous protein and has high water content. The chondrocytes are responsible for the synthesis and degradation of matrix components and are, therefore, ultimately responsible for the biomechanical and biologic properties of articular cartilage. Collagen (type II) produced by the chondrocytes accounts for more than half of the dry weight of adult articular cartilage. Individual collagen fibers, with a characteristic periodicity of 640 Å, vary from 300 to 800 Å in diameter, depending on their distance from the articular surface.
The principal component of the ground substance produced by chondrocytes is a protein polysaccharide complex termed proteoglycan. The central organizing molecule of proteoglycan is hyaluronic acid, with numerous glycosaminoglycans (mainly chondroitin sulfate and keratan sulfate) covalently bound from this central strand. Glycosaminoglycans carry considerable negative charge. The highly ordered array of electronegativity on the proteoglycan molecules interacts with large numbers of water molecules (small electric dipole). As a result, approximately 75% of the wet weight of articular cartilage is water, the majority of which is structured by the electrostatic forces of the proteoglycan molecule.
The structure of articular cartilage varies relative to its distance from the free surface. For the purposes of description, the tissue can be subdivided into three zones that run parallel to the articular surface ( Fig. 11-3 ). Electron microscopy of the free surface reveals a dense network of collagen fibers (40 to 120 Å in diameter) that is arranged tangentially to the load-bearing surface and at approximately right angles to each other. This dense, mat-like arrangement, the lamina obscurans , is acellular.
Zone 1, the superficial layer, contains large bundles of collagen fibers that are approximately 340 Å thick and lie parallel to the joint surface and at right angles to each other. This zone, the lamina splendens, has little or no intervening ground substance and contains the highest density of collagen. Chondrocytes in zone 1 are ellipsoid and are oriented parallel to the articular surface. Electron microscopy reveals little evidence of metabolic activity.
In zone 2 the collagen consists of individual, randomly oriented fibers of varying diameters. The chondrocytes in zone 2 tend to be more spherical and larger than those in zone 1, with abundant mitochondria and extensive endoplasmic reticulum, suggesting greater metabolic activity. The proteoglycan/collagen ratio in zone 2 is much higher than that near the surface.
In zone 3 the collagen fibers are thicker, often around 1400 Å in diameter, and tend to form a more orderly meshwork that lies radial to the articular surface. The chondrocytes in zone 3 are larger and tend to be arranged in columns, often appearing in groups of two to eight cells. The cells have been noted to have enlarged Golgi complexes, many mitochondria, and an extensively developed endoplasmic reticulum, indicating a high degree of metabolic activity.
Bone is a composite structure incorporating calcium hydroxyapatite crystals in a collagen matrix grossly similar to synthetic composites or to partially crystalline polymers. Devitalized bone provides a passive substratum for bacterial colonization as well as the ultimate incorporation of its proteinaceous and mineral constituents as bacterial metabolites. S. aureus binds to bone sialoprotein, a glycoprotein found in joints, and it produces chondrocyte proteases that hydrolyze synovial tissue.
Classification
Intra-articular sepsis may be classified in order of pathogenesis and frequency as direct hematogenous; secondary to contiguous spread from osteomyelitis; or secondary to trauma, surgery, or intra-articular injection ( Fig. 11-4 and Box 11-1 ). Most joint infections are caused by hematogenous spread, although direct contamination is not uncommon with trauma. Inoculation of the joint with bacteria can occur in association with the intra-articular injection of steroid, local anesthetic, or synthetic joint fluid. Infection rates following arthroscopy are low, ranging from 0.4% to 3.4%. Armstrong and Bolding reported that sepsis following arthroscopy could be associated with inadequate arthroscope disinfection and the use of intraoperative intra-articular corticosteroids. Tosh reported that inadequate sterilization caused an outbreak of Propionibacterium acnes from retained tissue within the arthroscope.
Hematogenous
Contiguous spread
- •
Osteomyelitis
- •
Soft tissue sepsis
- •
Vascular insufficiency
- •
Direct inoculation
- •
Surgery with or without a foreign body or biomaterials
- •
Trauma with or without a foreign body or biomaterials
- •
Osteomyelitis of the humerus can spread intra-articularly, depending on the age of the patient, the type of infecting organism, and the severity of infection. Osteomyelitis of the clavicle or scapula is uncommon, although it can occur after surgery and internal fixation, from retained shrapnel fragments, or in heroin addicts. Brancos and colleagues reported that S. aureus and P. aeruginosa were the etiologic agents in 75% and 11% of episodes, respectively, of septic arthritis in heroin addicts. The sternoclavicular joint was involved more commonly than the shoulder joint. Chaudhuri and colleagues have reported septic arthritis of the shoulder following mastectomy and radiotherapy for breast carcinoma. Lymphedema was present in all cases. The onset of infection was subacute in all cases, and delays in diagnosis led to destruction of the joint in all but one patient.
Hematogenous osteomyelitis, although common in children, is uncommon in adults until the sixth decade or later and is usually associated with a compromised immune system. Intravenous (IV) drug use is associated with the development of osteomyelitis in adults. Direct spread from wounds or foreign bodies, including total joint and internal fixation devices, is the most common etiology of shoulder sepsis in adults. Sepsis has been reported following shoulder arthrography, treatment for retroperitoneal abscess, and various gynecological surgeries. In 1959 Gowans and Granieri reported the relationship between intra-articular injections of hydrocortisone acetate and the subsequent development of septic arthritis. Kelly and colleagues reported that two of their six patients had a history of multiple intra-articular injections of corticosteroid. Ward and Goldner reported that chronic disease was present in more than half of their 30 cases of glenohumeral pyarthrosis and that four cases were associated with ipsilateral forearm arteriovenous dialysis fistulas. Soft tissue infection about the shoulder can also manifest in the form of pyomyositis, sometimes occurring as a result of hematogenous spread. Aglas and colleagues reported sternoclavicular joint arthritis as a complication of subclavian venous catheterization. Their two cases responded to antibiotic treatment. Glenohumeral pyarthrosis has been observed following acupuncture. Lossos and colleagues reported that associated medical conditions were present in the majority of their patients with septic arthritis of the shoulder.
Pathogenic Mechanisms of Septic Arthritis and Osteomyelitis
Surfaces as Substrata for Bacterial Colonization
The pathogenesis of bone and joint infections is related, in part, to the preferential adhesive colonization of inert substrata, such as the articular surface of joints or damaged bone, whose surfaces are not integrated with healthy tissue composed of living cells and intact extracellular polymers ( Fig. 11-5 ). Almost all natural biological surfaces are lined by a cellular epithelium or endothelium, with the exceptions being intra-articular cartilage and the surface of teeth. Mature enamel is the only human tissue that is totally acellular; it is primarily composed of inorganic hydroxyapatite crystals (96% by weight), with a small amount of water (3%) and an organic matrix (<1%). Cartilage and enamel are readily colonized by bacteria because they lack the protection by natural desquamation or by intact extracapsular polysaccharides that is provided by an active cellular layer. Their acellular surfaces are similar to many of those in nature for which bacteria have developed colonizing mechanisms. Certain strains of S. aureus adhere to specific sites on collagen fibrils, a process that is mediated by specific surface receptor proteins. Dissimilarities in surface structure are probably responsible for the specificity of bacteria species in colonizing these surfaces.
Enamel is mostly crystalline and inorganic, whereas cartilage is noncrystalline and organic. Enamel contains no collagen, whereas collagen is ubiquitous in cartilage and bone. S. aureus is the natural colonizer of cartilage, but not of enamel, because it contains collagen receptors. The specificity of colonization is also modulated in part by lectins and the host-derived synovial fluid, blood, and serum; by conditioning films of protein; and by polysaccharide macromolecules. The colonization of teeth by Streptococcus mutans and other organisms is a natural polymicrobial process and may be symbiotic or slowly destructive; however, bacterial colonization of articular cartilage is unnatural and rapidly destructive.
The acellular cartilage matrix and inanimate biomaterial surfaces offer no resistance to colonization by S. aureus and S. epidermidis , respectively. The observed invasion and gradual destruction of the cartilage over time supports clinical observations of the course of untreated septic arthritis ( Fig. 11-6 ). The acellular cartilaginous surfaces of joints are particularly vulnerable to sepsis because they allow direct exposure to bacteria from open trauma, surgical procedures, or hematogenous spread. This mechanism parallels previous observations on the mechanism of osteomyelitis, which suggest that the adhesion of bacteria to surfaces not protected by living cells, such as dead bone or cartilage, via receptors and extracellular polysaccharides is a factor in pathogenesis.
Intra-articular Sepsis
The articular cavity is a potential dead space that can provide a favorable environment for bacterial growth. In this avascular and relatively acellular space, host defense mechanisms are at a disadvantage. Synovial cells are not actively antibacterial, although they are somewhat phagocytic. White blood cells (WBCs) must be delivered to the area and lack a surface for active locomotion. Under such conditions phagocytic action is expected to be impaired, especially against encapsulated organisms.
Spontaneous intra-articular sepsis of the shoulder results from random hematogenous bacterial seeding. The synovial vasculature is abundant, and the vessels lack a limiting basement membrane. Bacteremia, especially caused by Neisseria gonorrhoeae , increases the risk of intra-articular spread. Nosocomial infections in neonatal intensive care units are usually related to the presence of intravascular devices. Contiguous spread from adjacent and intracapsular metaphyseal osteomyelitis also occurs. Surgery, arthroscopy, total joint replacement, aspirations, and steroid injections can also result in the direct inoculation of bacteria into the intra-articular space. The presence of foreign bodies from trauma or after surgery (stainless steel, chrome-cobalt alloys, ultra-high molecular weight polyethylene, and methylmethacrylate) increases the possibility of infection by providing a foreign body nidus for colonization, allowing antibiotic-resistant colonization to occur. The presence of a foreign body also decreases the size of the inoculant required for sepsis and perturbs the host’s defense mechanisms.
Septic arthritis of the shoulder most often involves the glenohumeral joint. The acromioclavicular and sternoclavicular joints are occasionally infected in specific patient groups or after steroid injections in arthritis. Direct contamination from open wounds is also possible. Sternoclavicular sepsis is more common in drug abusers and usually involves gram-negative organisms, specifically P. aeruginosa . The involvement of S. aureus , Escherichia coli , Brucella species, and N. gonorrhoeae has also been reported.
Septic arthritis of the shoulder has been reported to represent up to 14% of all septic arthritis cases. In earlier studies the incidence was 3.4%. Caksen and colleagues reported shoulder involvement in two of 49 joints involved in their series of pediatric patients with septic arthritis. A more elderly population, increased trauma, and the common use of articular and periarticular steroids may be the factors in this epidemiology. The primary causal organism of shoulder sepsis is S. aureus . Sepsis in immunocompromised patients may be polyarticular as well as polymicrobial. Ten percent of septic arthritis cases involve more than one joint, and it is likely to occur in children.
Osteomyelitis
Hematogenous osteomyelitis accounts for most cases of osteomyelitis in children. Contiguous osteomyelitis is more common in adults, secondary to surgery and direct inoculation. In patients older than 50 years, contiguous osteomyelitis and diseases related to vascular insufficiency are predominant. Of the bones of the shoulder, the humerus is most commonly involved in osteomyelitis. In drug abusers the clavicle is occasionally involved due to hematogenous spread. The scapula is rarely involved; usually infection occurs by direct inoculation or contiguous spread ( Fig. 11-7 and Table 11-1 ).
| Bacterial (Suppurative) | ||||
|---|---|---|---|---|
| Joint | Children * | Adults † | Mycobacterial | Viral |
| Knee | 41 | 48 | 24 | 60 |
| Hip | 23 | 24 | 20 | 4 |
| Ankle | 14 | 7 | 12 | 30 |
| Elbow | 12 | 11 | 8 | 20 |
| Wrist | 4 | 7 | 20 | 55 |
| Shoulder | 4 | 15 | 4 | 5 |
| Interphalangeal and metacarpal | 1.4 | 1 | 12 | 75 |
| Sternoclavicular | 0.4 | 8 | 0 | 0 |
| Sacroiliac | 0.4 | 2 | 0 | 0 |
* Data from Nelson JD, Koontz WC. Septic arthritis in infants and children: a review of 117 cases. Pediatrics. 1966;38:966-971; and Jackson MA, Nelson JD. Etiology and medical management of acute suppurative bone and joint infections in pediatric patients. J Pediatr Orthop. 1982;2:313-323.
† Data from Kelly PJ, Martin WJ, Coventry MD. Bacterial (suppurative) arthritis in the adult. J Bone Joint Surg Am. 1970;52:1595-1602; Argen RJ, Wilson DH Jr, Wood P. Suppurative arthritis . Arch Intern Med. 1966;117:661-666; Gifford DB, Patzakis M, Ivler D, Swezey RL. Septic arthritis due to Pseudomonas in heroin addicts. J Bone Joint Surg Am. 1975;57:631-635.
Epps and colleagues reviewed 15 patients with sickle cell disease and osteomyelitis affecting 30 bones. On culture of specimens of bone, S. aureus was isolated from eight of these patients, Salmonella species from six, and Proteus mirabilis from one. This suggests that Salmonella species are not always the principle causative organisms of osteomyelitis in patients with sickle cell disease.
Microbial Adhesion and Intra-Articular Sepsis
An understanding of microbial adhesion is required for complete clinical and therapeutic insight into joint sepsis. Studies of bacteria in marine ecosystems indicate that they tend to adhere in colonies to surfaces or substrata. The number of bacteria that can exist in a given environment is related directly to stress and nutrient supply. Surface attachment, rather than a floating or suspension population, is a favored survival strategy for bacteria; the major proportion of bacterial biomasses in most natural environments are therefore in an attached state, which is a common mode of microbial life in humans.
Bacterial attachment to surfaces is influenced by proteinaceous bacterial receptors and by an extracapsular exopolysaccharide substance—a biofilm—within which bacteria aggregate and multiply. Once bacteria develop a biofilm-enclosed adhesive mode of growth, they become more resistant to antiseptics, antibiotics, and host defense systems. Free-floating, nonadhesive bacteria or other microbes that lack a well-developed outer layer or exopolysaccharide are more susceptible to host-clearing mechanisms and to lower concentrations of antibacterial agents. Gibbons and van Houte first described the significance of this adhesive phenomenon in the formation of dental plaque. In diseases, such as gonococcal urethritis, cystic fibrosis, and endocarditis, bacterial colonization and propagation occur along endothelial and epithelial surfaces. The association between bacterial growth on biomaterial surfaces and infection was first described in 1963.
Microbial adhesion and associated phenomena also explain the foreign body effect, an increased susceptibility to infection experienced in the presence of a foreign body. Infections centered on foreign bodies are resistant to host defenses and treatment and tend to persist until the infecting locus is removed. Foreign bodies include implanted biomaterials, fixation materials, prosthetic monitoring and delivery devices, traumatically acquired penetrating debris and bone fragments, and compromised tissues.
Initial bacterial attachment or adhesion depends on the long-range physical force characteristics of the bacterium, the fluid interface, and the substratum. Specific irreversible adhesion, which occurs after initial attachment, is based on time-dependent adhesin-receptor interactions and on extracapsular polysaccharide synthesis. Biomaterial surfaces present sites for environmental interactions that result from their atomic structures ( Fig. 11-8 ). Metal alloys have a thin (100 to 200 Å) oxide layer that is the true biological interface. The surfaces of polymers and metals are modified by texture, manufacturing processes, trace chemicals, and wear debris and also by host-derived ionic, polysaccharide, and glycoproteinaceous constituents (conditioning films). The finite surface structure of conditioning films in humans is specific to each individual biomaterial, type of tissue cell, and local host environment. Tissue cells and matrix macromolecules also provide substrata for bacterial colonization. Bacteria have developed adhesins or receptors that interact with tissue cell surface structures ( Fig. 11-9 ).
Subsequent to or concomitant with the initial attachment, fimbrial adhesins (such as in E. coli ) and substratum receptors can interact, as in bacteria-to-tissue cell pathogenesis or for the glycoproteinaceous conditioning films that immediately coat implants. The production and composition of the extracellular polysaccharide polymer, which tends to act like a glue, is a pivotal factor. After colony maturation, cells on the periphery of the expanding biomass can separate or disaggregate and disperse, a process moderated by colony size, nutrient conditions, and hemodynamic or mechanical shear forces. In natural environments disaggregation is a survival strategy for the bacteria; in humans, however, it is involved in the pathogenesis of septic emboli. Disaggregation (dispersion) and its parameters might explain the phenomenon of intermittent or short-term bacterial showers or disseminated bacterial emboli.
Bacterial Pathogens
Organisms involved in septic arthritis and osteomyelitis of the shoulder include, in order of frequency, S. aureus, S. epidermidis, Streptococcus group B, E. coli, P. aeruginosa, Haemophilus influenzae type B, N. gonorrhoeae, Mycobacterium tuberculosis, Salmonella and Pneumococcus species, and Yersinia enterocolitica. Reported associations and other etiologic pathogens are listed in Box 11-2 .
Bacteria
Staphylococcus aureus
Staphylococcus epidermidis, Streptococcus group B
Escherichia coli, Pseudomonas aeruginosa, Haemophilus influenzae type B, Neisseria gonorrhoeae, Mycobacterium tuberculosis, and Salmonella and Pneumococcus species
Yersinia enterocolitica
Fungi
Actinomyces species
Blastomyces species
Coccidioides species
Candida albicans
Sporothrix schenckii
Reported Associations
Rheumatoid arthritis: Listeria monocytogenes
Renal transplant: Aspergillus fumigatus
Newborns and pregnant women: group B β-hemolytic Streptococcus agalactiae
Lymphedema: Pasteurella multocida
Septic arthritis in systemic lupus erythematosus: Mycobacterium xenopi
Chronic vesicoureteral reflux: Escherichia coli
Sickle cell disease: Salmonella group G
S. aureus is now the most common cause of septic arthritis in children, followed by group A Streptococcus , and Enterobacter species. H. influenzae , previously a concern in those younger than 2 years, has significantly decreased with vaccination. The identification of Kingella kingae isolates in septic joints has increased with improved testing. Lavy and colleagues reported on 19 children under the age of 2 years with Salmonella septic arthritis of the shoulder. They concluded that low nutritional status was a factor in the development of bacteremia in their patients. Hematogenous septic arthritis in infants is primarily streptococcal, whereas hospital-acquired infections are primarily staphylococcal but can also feature Candida and gram-negative organisms, especially in infants.
S. aureus is most common cause of septic arthritis in adults; N. gonorrhoeae is common in adults younger than 30 years. Hemolytic streptococci are the most common streptococci in adults and children. Group B β-hemolytic streptococcal infection may rarely be associated with necrotizing fasciitis and death. Necrotizing fasciitis has also been reported to be caused by S. aureus. Clostridium septic arthritis has been reported to develop spontaneously and following intra-articular steroid injection.
Gram-negative bacilli, such as E. coli and P. aeruginosa , are found in approximately 15% of joints and are especially prevalent in patients with urinary tract infections, diabetes, or a debilitating disease. Pseudomonas sternoclavicular pyarthrosis is associated with IV drug abuse. M. tuberculosis involves the knee, hip, ankle, and wrist more commonly compared with the shoulder. Mycobacterium marinum is found in marine environments. Blastomyces usually spreads from osteomyelitis to the intra-articular space. Candida albicans can spread via the hematogenous route in debilitated patients or directly from steroid injections. Shoulder girdle abscess formation due to Streptococcus agalactiae has been described as a complication of esophageal dilation. Aspergillus arthritis of the glenohumeral joint has been reported in a renal transplant patient with associated neurologic involvement. Neutropenia and corticosteroid therapy have been associated with immunodeficiency-inducing risk factors. Pneumococcal septic arthritis seems to be predominantly a disease that affects the elderly.
S. aureus is often the major pathogen in biometal, bone, joint, and soft tissue infections and is the most common pathogen isolated in osteomyelitis when damaged bone or cartilage acts as a substratum. The predominance of S. aureus in adult intra-articular sepsis may be explained by its ubiquity as a tissue pathogen seeded from remote sites, its natural invasiveness and toxicity, and its receptors for collagen, fibronectin, fibrinogen, and laminin. S. epidermidis is most often involved when the biomaterial surface is a polymer or when a polymer is a component of a complex device (extended-wear contact lenses, vascular prostheses, and total joint prostheses). S. epidermidis, S. aureus, and Propionibacterium species are the most common organisms associated with deep infection following rotator cuff repair.
Studies of chronic adult osteomyelitis have revealed polymicrobial infections in more than two thirds of cases. The most common pathogens isolated include S. aureus and S. epidermidis , and Pseudomonas , Enterococcus , Streptococcus , Bacillus , and Proteus species. Polymicrobial infections, therefore, appear to be an important feature of substratum-induced infections; they are probably present more often than is realized, and can be a feature of chronic intra-articular sepsis and sinus formation.
In summary S. aureus is the most common organism in septic infections and is usually spread via hematogenous seeding. S. epidermidis is the principal organism in biomaterial-related infections, especially those centered on polymers. Mixed (polymicrobial), gram-negative, and anaerobic infections are often associated with open wounds and sinus tracts.
Clinical Presentation
Symptoms and Signs
Pain, loss of motion, and effusion are early signs of infection. However, shoulder effusion is difficult to detect and is often missed. Motion is painful, and the arm is adducted and internally rotated. Radiographs might show a widened glenohumeral joint space and later signs of osteomyelitis ( Fig. 11-10 ). Systemic signs include fever, leukocytosis, and sedimentation rate changes. The symptoms of immunosuppressed and rheumatoid patients may be muted. Delay in presentation is common, averaging greater than 7 days. In a 50-patient case series by Sperling and colleagues, eight showed bilateral infection.
The sternoclavicular joint may be involved and should be suspected in unilateral enlargement without trauma in patients younger than 50 years. Gonococcal and staphylococcal infections have been reported. IV drug abusers are susceptible to infection by gram-negative organisms, especially P. aeruginosa and Serratia marcescens . The acromioclavicular joint is rarely involved in sepsis but may be contaminated by steroid injections. Wound infection is not uncommon after surgical resection of the distal clavicle for osteoarthritis, probably due to the proximity of the joint to the overlying skin and the lack of an intervening muscle layer. Chanet and colleagues reported that a past history of radiation for breast cancer was a risk factor for the development of septic arthritis of the glenohumeral and sternoclavicular joints. The mean time elapsed since radiation was 16 years (range, 3 to 34 years).
Gabriel and colleagues reported on a 5-week-old boy who had a brachial plexus neuropathy and paralysis of the upper extremity secondary to septic arthritis of the glenohumeral joint and osteomyelitis of the proximal part of the humerus. They pointed out that pseudoparalysis of a limb associated with sepsis was a well-documented phenomenon. Similarly, muscular spasm associated with pain caused by infection can lead to apparent weakness. True nerve paralysis associated with osteomyelitis is uncommon, and its documentation by electrodiagnostic studies is rare. Permanent weakness persisted in the patient even though the glenohumeral joint and proximal humerus were surgically drained. The possible causes of the plexus neuropathy associated with infection included ischemic neuropathy from thrombophlebitis of the vasa nervorum, arterial embolism, hyperergic or hypersensitivity reactions, and local compression due to abscess formation. Rankin and Rycken reported bilateral dislocations of the proximal humerus as a result of septic arthritis. Miron and colleagues have also reported transient brachial plexus palsy associated with suppurative arthritis of the shoulder.
Total Shoulder Replacement
Sepsis after total joint replacement of the shoulder is relatively rare because of prophylactic antibiotic use and the excellent blood supply of the surrounding soft tissues. Symptoms of infection include pain, loss of motion, and subluxation. Pain relief is so universal after total shoulder replacement that infection should be suspected if there is pain or lucency around the cement mantle.
Rheumatoid Arthritis
Patients with chronic rheumatoid arthritis are susceptible to spontaneous septic arthritis. Because the active destructive process of the rheumatoid arthritis masks the septic condition, detection of the infection is often delayed. The onset of septic arthritis should be suspected when the clinical course of the rheumatoid patient worsens acutely, especially if the disease is long term. When infection is present, the patient experiences a sudden aggravation of pain as well as swelling and increased temperature in the joint; sudden chills can also occur. The physician should emphasize to patients with chronic rheumatoid arthritis (and to caregivers) that a sudden exacerbation of symptoms warrants investigation.
Differential Diagnosis
Radiographs are not especially useful in the early diagnosis because septic arthritis does not significantly alter the bone destruction resulting from rheumatoid arthritis and because bone and joint radiographic changes are delayed. Other acute arthritic disorders can imitate or mask sepsis, including gout, pseudogout, rheumatic fever, juvenile rheumatoid arthritis, neuropathic arthropathy, and the oligoarthritic syndromes. Trauma and tumors can cause adjacent joint effusions and must be considered.
Laboratory Evaluation
The culture and analysis of synovial fluid is critical for diagnosis. The joint should always be aspirated when sepsis is suspected. Radiographic control is indicated if the approach is difficult about total joints. The injection of saline or simultaneous arthrography of the glenohumeral joint may be helpful in certain cases. When the results of cultures are negative and the diagnosis is difficult to make, an arthroscopic biopsy can be useful. A synovial biopsy and culture for acid-fast organisms and fungi should be performed in patients with chronic monoarticular arthritis, especially those with tenosynovitis.
Viral infection must be considered when bacteria cannot be identified. Smith and Piercy report that viral arthritis is associated with rubella, parvovirus, mumps, hepatitis B, and lymphocytic choriomeningitis. For a patient who presents with multiple joint involvement and systemic manifestations consistent with a viral infection, serologic confirmation of the infection should be obtained because it is not usually possible to isolate the virus from joint fluid.
Synovial Fluid Analysis
If septic arthritis is suspected, the synovial fluid should be examined. Septic arthritis is probable if the leukocyte count is greater than 50,000 cells/mm 3 , the glucose level is low, and more than 75% of the cells are polymorphonuclear. These findings are beyond the range compatible with uncomplicated rheumatoid arthritis. In bacterial infections aspiration can yield 10 mL or more of fluid. Synovial joint fluid is usually opaque or brownish, turbid, and thick, but it may be serosanguineous in 15% of cases with poor mucin clot formation. Proteins are elevated primarily because of an elevated WBC count (usually >50,000/mm 3 and often as great as 100,000/mm 3 , primarily of neutrophils). Half of adults and a less than half of children have a glucose level in the joint fluid that is 40 mg/L less than that in the serum glucose drawn at the same time. These findings are more common later in infection. Polymorphonuclear leukocytes are dominant (90%); counts greater than 100,000/mm 3 are typical of staphylococcal and acute bacterial infection. Mehta and colleagues reported positive cultures in 96% of aspirates from patients with suspected septic arthritis when the polymorphonuclear differential count was greater than 85% of the total aspirate WBC count. Monocytes are more predominant in mycobacterial infections. Crystal examination is needed to rule out gout or pseudogout. Rheumatoid, rheumatic, and crystalline joint diseases also elevate leukocytes, but the presence of these diseases does not exclude concomitant sepsis.
The results of Gram staining are positive approximately 50% of the time, but false-positive results do occur. Positive joint cultures occur in 90% of patients with established bacterial septic arthritis and in 75% of patients with tubercular arthritis. Blood cultures should also be obtained; the results are positive in approximately 50% of patients with acute infection. Some prosthesis-centered infections are difficult to detect unless tissue is biopsied and prepared for culture ( Table 11-2 ). Protocols may need adjustment to allow adequate growth time to identify slower growing organisms, such as P. acnes . The current recommendations for isolating P. acnes state that it requires at least 13 days after collection. Culture specimens should be taken for gram-positive, gram-negative, aerobic, and anaerobic bacteria, and for mycobacteria and fungi. Laboratory technique and media selection should be based on the type of antibiotic given to the patient and on the specific nutrient requirements of suspected bacteria. The magnitude of anaerobic septic arthritis has been underestimated in the past.
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