Hematogenous dissemination from another organ system, such as skin breakdown, urinary system infections, or pneumonia, is
the most common. In over 50% of the patients with intraarticular sepsis, there is a positive blood culture.⁴⁷ Goldenberg and Cohen isolated the pathogen from a distant focus in 50% of the cases.

Similar to the findings reported by Chung in the hip,¹⁸ in the shoulder, branches of the suprascapular and subscapular arteries, along with the anterior and posterior circumflex humeral arteries, form an extracapsular arterial ring, which supplies the proximal humerus (Fig. 35-1A,B).⁴¹ This anastomosis gives off branches that penetrate the capsule and form an intraarticular synovial ring.⁵⁸ This has been termed the “transition zone” and is located between the synovium and the articular surface.¹⁰² It is in this area that the arterioles loop acutely toward the periphery, creating a low-flow state, making the area more susceptible to receptor-specific interaction of the pathogen and the cell surface.

Spontaneous shoulder sepsis is the result of joint invasion during bacteremia. Septic arthritis has been shown to occur in experimental animals when bacteremia is created.⁷⁶ The abundance of the synovial vasculature and the absence of a basement membrane between the endothelial cells make synovial joints vulnerable to seeding by bacteria. Furthermore, most patients with hematogenous nongonococcal bacterial arthritis have at least one underlying chronic medical risk factor. These factors may be local, such as prosthetic and metallic implants, or they may be systemic, such as cancer, cirrhosis, rheumatoid arthritis, and intermittent bacteremic episodes from intravenous drug abuse or indwelling catheters⁴⁸ (Table 35-1).

Direct inoculation may be traumatic or iatrogenic. Repeated injections, arthroscopy, and open surgical procedures, such as rotator cuff repair and arthroplasty, have been shown to be associated with pyarthrosis of the shoulder. The incidence of infection following intraarticular steroid injection is extremely small. Hollander reported 18 infections in 250,000 injections,⁶³ and Gray et al. found only two cases complicating 100,000 injections⁵⁰ The advent of sterile disposable needles and syringes and adherence to meticulous aseptic technique has helped lessen the risk. The existence of foreign bodies around the joint or devitalized bone from trauma can provide a nidus for adhesion and colonization by bacteria.⁵²,⁵⁶,⁵⁸ This nidus allows a glycocalyx biofilm to be expressed by the bacteria, which contributes to antibiotic resistance and limits the effectiveness of the immune response of the host.

Osteomyelitis is most often hematogenous in origin and, in particular, is a disease of young children and the elderly. Hematogenous osteomyelitis commonly involves the metaphyseal area of rapidly growing long bones, usually occurring in the hip and knee.⁸⁴ When septic arthritis results from a contiguous infection such as osteomyelitis, it spreads from the bone to the synovium, then to the joint space. This happens most often in infancy, when there is a vascular anastomosis between the epiphysis and the metaphysis. Studies conducted on the proximal femur by Trueta¹¹⁵ showed a direct vascular communication between metaphyseal arterioles and the epiphyseal ossicle before 8 months of age. This allows a direct hematogenous communication between an osteomyelitis of the metaphysis and the adjacent joint synovium.²⁹,⁸⁷ Between the ages of 8 and 18 months, the last vestiges of the nutrient artery system close down at the growth plate. The open physis at this point provides an effective barrier to the spread of infection to the joint by obliterating this vascular anastomosis.¹⁰⁹ This situation is analogous in the proximal humerus.

At skeletal maturity, there is once again a direct osseous connection between the metaphysis and epiphysis, secondary to closing of the growth plate and reestablishment of anastomoses between the metaphyseal and epiphyseal arterioles.³ Therefore, infection of the proximal humeral metaphysis may extend to the epiphysis and the joint through the haversian system and Volkmann canals. In addition, the proximal 10 to 12 mm of the metaphysis of the proximal humerus is intraarticular, giving the pathogens of metaphyseal osteomyelitis direct access to the synovium.

The anatomy of the shoulder joint is intricately involved in the pathogenesis of sepsis. All synovial joints contain synovial fluid, which can act as an excellent growth medium for bacteria and have a relative lack of immunologic resistance.³⁶ Type B synoviocytes are weakly phagocytic but in most cases are able to limit and clear a blood-borne bacterial infection.⁶ Therefore, there must be an imbalance between normal synovial cell function and the invading bacteria for an intraarticular infection to develop.

Synovial tissue is relatively resistant to infection.⁶ Examination of joints in which experimental septic arthritis has been produced reveals infrequent colonization of the synovium.¹¹⁹ Receptors for collagen have been found on several strains of Staphylococcus aureus. It may be a lack of ligands or a functional host resistance mechanism that helps to prevent synovial colonization.⁵⁸

Microscopic examination of the synovium shows that it is relatively thin in the area of the transition zone, rarely being more than three or four cell layers thick. The synovial capillaries are superficial, making them more susceptible to trauma. The lack of epithelial tissue in the synovium, and thus the lack of a basement membrane, means that there is no structural barrier to the spread of bacteria from the synovium to the joint. Thus, transient bacteremia and trauma causing intraarticular hemorrhage can play a role in the pathogenesis of septic arthritis.⁵⁸

Integral to the pathogenesis of infectious arthritis is the preferential colonization of bacteria to articular cartilage, traumatized bone, or biomaterials that are not integrated with healthy tissues composed of living cells and extracellular matrix proteins.¹⁰,⁵⁶,⁵⁸,¹⁰⁵,¹¹⁰ Bacterial adhesion involves either very specific receptor-ligand or receptor-lectin-ligand chemical interaction or nonspecific interaction based on charge-related, hydrophobic, and extracellular polysaccharide-based interactions.⁵⁵ S. aureus has receptors for types I and II collagen,¹⁰⁸ fibrinogen, laminin, fibronectin, thrombospondin, bone sialoprotein, and heparin sulfate.¹⁰⁶ Many factors influence the adherence properties of bacteria, including (a) the surface energy and surface-free energy of the bacteria and biomaterial, (b) the extracellular components of the bacteria, (c) the bacterial interaction in mixed infections, (d) the host immune system, and (e) the extracellular matrix.³⁴

All natural, biologic surfaces, with the exception of teeth and articular cartilage, are protected by the epithelium, endothelium, or periosteum, which decreases bacterial adhesion by desquamation or by the presence of host extracellular polysaccharide molecules. S. aureus is the natural colonizer of cartilage and collagen, because it has specific surface-associated adhesins²⁶ for sites on collagen, not for enamel. Although the colonization of teeth by Streptococcus mutans is a natural symbiotic process that can be slowly destructive, the bacterial colonization of articular cartilage is unnatural and is rapidly destructive.⁴²,⁵⁸ Bacterial adherence is characterized by the production of an extracellular exopolysaccharide, within which the bacteria aggregate and multiply. Bacteria in aquatic environments grow predominantly in these biofilm-enclosed microcolonies adherent to surfaces.⁵³ Following initial colonization, the microcolonies develop coherent and continuous biofilms³⁶ that contain more than 99.9% of the bacteria in thick layers, within which they are protected from antibacterial agents²⁴,⁵³,⁵⁴ and the host immune defenses. This glycocalyx allows the bacteria to modify their local environment, limiting both the specific and the nonspecific arms of the immune response. Bacteria adherent to bone, methyl methacrylate, orthopedic devices, and surrounding tissue are harder to completely eradicate until the infected tissue and biomaterial are removed. Not infrequently, the infections are polymicrobial and difficult to culture adequately, unless special techniques are used.⁴⁴,⁴⁷,⁵²,⁵⁴,⁵⁵

Patient age and host states help predict the bacterial cause of septic arthritis. Those organisms that frequently cause bacteremia in certain age groups are usually the infecting organisms, since joint sepsis is most commonly caused by hematogenous seeding. However, certain organisms, such as Neisseria gonorrhoeae and S. aureus, seem to have an avidity for the synovium, causing septic arthritis out of proportion to their incidence of bacteremia.¹⁰⁹ S. aureus is the most common cause of adult,
nongonococcal bacterial arthritis, occurring in up to 50% of patients.⁷⁴ Ward and Goldner¹²¹ noted 77% of infecting organisms to be Gram positive, of which 46% were S. aureus. Propionibacterium acnes is an anaerobic, Gram-positive bacillus that is found in lipid-rich areas, such as hair follicles and sebaceous glands, and in moist areas, such as the axilla. Although it is rarely the causal organism in other large joint infections, P. acnes has frequently been reported as the offending pathogen in shoulder sepsis and should not be dismissed as a skin contaminant. Joint infections with Gram-negative bacilli have been increasing in incidence, ranging from 5% to 30% of all shoulder infections.³³,⁴⁰,⁷⁴,¹¹³ They most often occur in patients with intravenous drug abuse, malignancy, diabetes, immunosuppression, or hemoglobinopathy.¹⁰⁹ Escherichia coli and Proteus species are common infecting Gram-negative organisms from the urinary tract, and occur in patients who are not intravenous drug abusers. Although Pseudomonas and Serratia are the common organisms in intravenous drug addicts, the incidence of S. aureus in this population has been increasing.⁵,¹¹,³³ Streptococcus pneumoniae is the most common organism in patients with chronic alcoholism and hypogammaglobulinemia.⁸⁵ Polymicrobial infections of the shoulder occur in 5% to 15% of patients, often associated with an extraarticular polymicrobial infection or penetrating trauma, especially in immunocompromised patients.⁹⁵

The incidence of shoulder sepsis is increasing as the population ages and the prevalence of chronic, debilitating disease increases.⁷⁴,¹¹³ Currently, primary shoulder sepsis accounts for 10% to 15% of all joint infections, whereas the hip and the knee account for 20% to 25% and 40% to 50%, respectively.³³ Septic arthritis of the shoulder is a rare occurrence in the young, immunocompetent person. More frequently, it is a disease of the elderly.¹¹⁸ Most patients have chronic, systemic, immunocompromising conditions such as diabetes mellitus, blood dyscrasias, renal failure, malignancy, and malnutrition.³⁴,⁴⁷,⁷⁴,¹²¹ Local factors also play a role in some patients, such as indwelling catheters, intravenous drug use, prior joint disease (rheumatoid or osteoarthritis), trauma, bursitis, or radiation therapy.³⁴,⁴⁸,¹⁰⁹ Ward and Goldner reported that 74% of 27 adults with septic arthritis of the shoulder had some systemic condition causing immunocompromise or some type of local tissue abnormality. In 52% of the patients, both were present.¹²¹