Mycobacterium tuberculosis infection of the shoulder is an unusual condition, with few cases reported in the orthopaedic literature. Although skeletal tuberculosis is uncommon in developed countries, several conditions, of which the orthopaedic surgeon should be aware, predispose patients to mycobacterial shoulder infections. We report a case of Mycobacterium tuberculosis infection of the shoulder that occurred thirty-seven years after a shoulder hemiarthroplasty. The patient was informed that data concerning the case would be submitted for publication, and he consented.
A seventy-four-year-old man who had a history of left-shoulder posttraumatic arthritis that had been treated thirty-seven years previously with a Neer hemiarthroplasty presented with left shoulder pain, swelling, and induration along with intermittent fever. The medical history was notable for the diagnosis of a gastrointestinal stromal tumor that required multiple debulking resections of the small bowel and liver along with resections of retroperitoneal and subdiaphragmatic metastatic lesions. The patient was undergoing long-term chemotherapy with Sutent (sunitinib malate) for the treatment of extensive metastasis to the liver. At initial presentation, the patient reported that his left shoulder had functioned well except for mild pain and limitations with repetitive overhead activity. His shoulder symptoms had worsened over the preceding three weeks. Physical examination demonstrated intact shoulder motor function along with erythema and fullness in a painful left shoulder. The rotator cuff was intact. Radiographs of the left shoulder revealed a well-aligned hemiarthroplasty without evidence of implant loosening but with moderate glenoid erosion. Magnetic resonance imaging (MRI) and computed tomography (CT) scan of the shoulder were not acquired, but a CT scan of the chest, abdomen, and pelvis acquired two months earlier for surveillance of known gastrointestinal stromal tumor demonstrated mild to moderate glenoid erosion. During his initial hospitalization, the patient underwent two irrigation and debridement procedures of the left shoulder for a suspected abscess.
At the time of the initial debridements, there was frank pus superficial to the joint capsule and the abscess did not clearly involve the shoulder joint or humeral implant. Routine bacterial and fungal cultures from the shoulder revealed no growth, and the patient was empirically treated at home with six weeks of intravenous vancomycin (via a peripherally inserted central catheter [PICC line]), and a suppressive oral Bactrim (trimethoprim and sulfamethoxazole) regimen, as recommended by the infectious disease consultant. The patient had no known history of Mycobacterium tuberculosis infection or exposure. He did not travel to any areas endemic for tuberculosis, nor did he have any family members with tuberculosis infection. Neither human immunodeficiency virus (HIV) testing nor mycobacterial cultures were ordered at the time of the initial two surgical debridements.
The patient was referred to us five months after the initial irrigation and debridement. At that time, two draining fistulas were present at the site of the prior incision (Fig. 1), and the patient's chief complaints were pain, reduced shoulder motion, and general malaise. The results of laboratory studies included a persistently elevated erythrocyte sedimentation rate in the range of 40 to 80 mm/hr (normal values, 0 to 29 mm/hr). Radiographs showed implant subsidence and lucencies (Fig. 2). The patient underwent irrigation and debridement, deep-tissue cultures and biopsy, implant removal, and placement of an antibiotic cement spacer (Fig. 3). Bacterial cultures were incubated for fourteen days and revealed growth of coagulase-negative, beta-lactamase-negative Staphylococcus. The patient was initially treated with intravenous vancomycin under the guidance of an infectious disease specialist. Six weeks postoperatively, the cultures for Mycobacterium tuberculosis were positive in one of three specimens. The results of the initial acid-fast bacillus test were negative. Histologic examination of the tissue biopsy demonstrated caseating granulomas that were consistent with tuberculosis.
The state health department was contacted so that all healthcare workers, staff, and patients who may have had contact with the patient could be contacted and advised to undergo exposure screening. The patient was admitted to the hospital and placed in isolation. HIV testing was negative at that time. Three sputum cultures were all negative for pulmonary tuberculosis, and the patient was discharged home. Eight weeks after the prosthesis was removed, shoulder drainage resumed. The patient underwent extensive debridement without wound closure and underwent treatment with a wound vacuum-assisted closure system. Cultures were positive for methicillin-resistant Staphylococcus aureus. The wound ultimately healed after five weeks and remained closed with a retained antimicrobial-loaded cement spacer in the shoulder.
The patient was subsequently treated with the classic four-drug regimen for tuberculosis (rifampin, isoniazid, pyrazinamide, and ethambutol). After sensitivity studies revealed the mycobacterium isolate to be susceptible to all of the drugs, the patient was switched to a two-drug regimen consisting of rifampin and isoniazid for a total treatment course of ten months. He was also treated with vancomycin for approximately three months for the bacterial infection.
At the time of the last follow-up, the patient had no pain but had reduced motion and function in the left shoulder with the spacer in place. Potential reconstructive options were discussed but, due to minimal functional requirements and planned transfer to long-term hospice care because of issues related to progression of the gastrointestinal stromal tumor, the patient declined further orthopaedic intervention. The patient died as a result of complications from cancer eighteen months after the prosthesis was removed.
Nearly 13,000 cases of tuberculosis were reported in the United States in 2008. Although there had been a surge in the prevalence of tuberculosis in the U.S. during the 1980s, the total reported cases of tuberculosis infections have slowly decreased since 19921. Tuberculosis still remains one of the most common infections and one of the most common causes of death associated with HIV infection1,2. The advent and administration of antiretroviral medications for the treatment of HIV have contributed to this decreased prevalence. Almost one-third of the world's human population is infected with tuberculosis and nearly 9 million people become ill with tuberculosis each year1. In the U.S., mycobacterium infection involving joints is uncommon, with the majority of published cases involving infections about a total joint prosthesis of the hip, the knee, and, more rarely, the shoulder3-6. Nontubercular mycobacterium infections of the shoulder as well as other joints have also been described in varying degrees in the infectious disease, rheumatologic, and orthopaedic literature7,8. Rare case reports from Japan have described tuberculosis of native shoulders9, and the Korean orthopaedic literature has described Mycobacterium tuberculosis infection of the subdeltoid bursa along with rice body formation in a native shoulder10. Overall, extrapulmonary involvement of tuberculosis infection is found in 20% of patients with tuberculosis, with reported involvement of the shoulder in less than 2% of these individuals11,12.
The case of our patient demonstrates the importance of maintaining a high suspicion of atypical organisms when treating musculoskeletal infections in patients who have an atypical medical history. While most patients with tubercular infections have a prior history of tuberculosis or have been in close contact with a person who has tuberculosis, our patient represents the chronically immunosuppressed patient who is at risk of developing mycobacterial diseases. This patient's history of gastrointestinal stromal tumors and associated chemotherapy treatments provided key historical elements to the case that could have helped to better guide the initial diagnostic studies.
As reported in other case studies involving joint infections caused by Mycobacterium tuberculosis, another indication of a possible mycobacterial organism was the history of negative bacterial and fungal cultures. While initial tests included evaluation for the presence of fungus, the immunosuppressed state of our patient may have been a reason for a more extensive search for atypical organisms. The history of negative bacterial and fungal cultures as well as the continued presence of symptoms that were consistent with infection despite treatment strongly suggests the presence of an atypical organism. Additionally, the presence of a sinus track has been noted as being characteristic of an atypical infection3.
At the time of debridement and prosthesis removal, three tissue samples were sent for laboratory evaluation of bacterial, fungal, and acid-fast species. Only one of the three samples grew acid-fast isolates, and none of the tissue samples revealed acid-fast species with use of Gram stains. This further reinforces the clinical importance of obtaining multiple intraoperative tissue samples from patients with atypical infections so that diagnostic accuracy will be improved. A high index of suspicion of atypical etiologies should be maintained, regardless of the presence or absence of frank pus within the wound or in the joint. Although the prevalence of tuberculosis in the U.S. has been slowly decreasing, it is still likely that most practicing orthopaedic surgeons will encounter and treat a patient with tuberculosis. The surgeon must maintain a high index of suspicion to avoid a delay in diagnosis and increased morbidity. In addition to patients who have migrated from countries in which there is a high prevalence of tuberculosis or patients who have had prior septic arthritis caused by Mycobacterium tuberculosis, our patient represents another subset of patients who remain at risk for tuberculous joint infections. Immunosuppressed patients, whether their immunosuppressed state is due to HIV, chemotherapy, congenital conditions, increased age, or long-term corticosteroid use, are at risk for typical and atypical infections, and the treating physician should consider the possibility of mycobacterial causes when managing patients with septic arthritis. The presence of caseating granulomas should further increase the index of suspicion for atypical infection.
In conclusion, the authors recommend continued testing for mycobacterial infections during treatment for a suspected infection about a prosthesis, particularly in the presence of a draining sinus or in a patient with a compromised immune system.