Orthopedics

Feature Article 

Atypical Mycobacterial Infections of the Upper Extremity

Kevin P. Smidt, BS; Peter J. Stern, MD; Thomas R. Kiefhaber, MD

Abstract

Atypical mycobacterial infections of upper extremity synovial-lined structures are often misdiagnosed and unrecognized. Despite an increasing incidence, lack of physician awareness of these pathogens may result in considerable delay in diagnosis and management, potentially leading to permanent disability. The authors conducted a literature review and analyzed 31 cases of penetrating atypical mycobacterial infection to better understand the clinical characteristics and to evaluate their posttreatment complication rate compared with available literature. Medical records for culture-positive cases of tenosynovial or intra-articular atypical mycobacterial infections of the upper extremity that were treated were retrospectively reviewed. Treatment outcomes were analyzed against published case reviews and case series. Thirty-one cases of penetrating atypical mycobacterial infection were identified. Mycobacterium marinum (n=11) was the most common organism and was associated with aquatic exposure. Twenty-eight cases received empiric treatment, 17 of which received contraindicated treatment. Patients saw an average of 5 physicians prior to receiving an accurate diagnosis, and the mean time to diagnosis was 10 months. All cases received antibiotic treatment in addition to surgical management. Twenty cases (68%) failed treatment outcomes. Delay in diagnosis and inappropriate management of atypical mycobacterial infections may lead to a treatment failure rate that is higher than what has been reported in the literature. Mycobacterium avium and M fortuitum had significantly higher failure rates than other organisms. A high index of suspicion is required to make a diagnosis and prevent residual disability. [Orthopedics. 201x; xx(x):xx–xx.]

Abstract

Atypical mycobacterial infections of upper extremity synovial-lined structures are often misdiagnosed and unrecognized. Despite an increasing incidence, lack of physician awareness of these pathogens may result in considerable delay in diagnosis and management, potentially leading to permanent disability. The authors conducted a literature review and analyzed 31 cases of penetrating atypical mycobacterial infection to better understand the clinical characteristics and to evaluate their posttreatment complication rate compared with available literature. Medical records for culture-positive cases of tenosynovial or intra-articular atypical mycobacterial infections of the upper extremity that were treated were retrospectively reviewed. Treatment outcomes were analyzed against published case reviews and case series. Thirty-one cases of penetrating atypical mycobacterial infection were identified. Mycobacterium marinum (n=11) was the most common organism and was associated with aquatic exposure. Twenty-eight cases received empiric treatment, 17 of which received contraindicated treatment. Patients saw an average of 5 physicians prior to receiving an accurate diagnosis, and the mean time to diagnosis was 10 months. All cases received antibiotic treatment in addition to surgical management. Twenty cases (68%) failed treatment outcomes. Delay in diagnosis and inappropriate management of atypical mycobacterial infections may lead to a treatment failure rate that is higher than what has been reported in the literature. Mycobacterium avium and M fortuitum had significantly higher failure rates than other organisms. A high index of suspicion is required to make a diagnosis and prevent residual disability. [Orthopedics. 201x; xx(x):xx–xx.]

Atypical mycobacteria, also known as nontuberculous mycobacteria, were classified by Runyon1 in 1959 into 4 groups based on their growth rate and colony pigmentation. Although some atypical mycobacteria are restricted to certain environments, many others are ubiquitous.2 Environmental contact is often thought to be the source of infection, particularly aquatic exposure.3 Ninety percent of clinical infections cause disease in the pulmonary system, while other manifestations may involve the lymph nodes, skin, soft tissue, and bone.2

Although rare, atypical mycobacterial infections (AMIs) of synovial-lined structures, such as joints and tendons, in the upper extremity cannot be overlooked.3 A high index of suspicion is required for proper diagnosis, which is often missed or delayed because of lack of awareness or knowledge of these pathogens.4 Other barriers to clinical diagnosis include difficulty in organism isolation and an indolent clinical course.3 Thus, when evaluating chronic hand infections, cultures for atypical mycobacteria should be performed in addition to staining for acid-fast bacteria.5 Misdiagnosis or delayed diagnosis may result in a delay of appropriate management, leading to permanent disabilities.6 Noteworthy risk factors for these infections include immunodeficiency, diabetes, and the job titles of marine worker and farmer.7

Options for treatment of subcutaneous upper extremity infections include antibiotic treatment alone, radical surgical debridement alone, or a combination of antibiotic treatment and surgical debridement.8–12 All treatment modalities have shown some success, although current recommended treatment for invasive mycobacterial infections includes a combination of surgical debridement and antibiotic treatment.10,13 Surgical management generally involves multiple surgeries, including debridement, excision, synovectomy, and tenosynovectomy.10 If left untreated, subcutaneous AMIs can lead to locally penetrating infections or systemic infections that are much more difficult to treat.13

The authors conducted a retrospective case review of AMIs to gain a better understanding of their clinical course and to evaluate posttreatment complications. The authors hypothesized that these infections may be incurable, result in posttreatment complications, and culminate in permanent, residual disability.

Materials and Methods

The authors identified patients 18 years or older presenting to either the TriHealth Hand Surgery Center or the University of Cincinnati Medical Center from 1989 to 2014 who were diagnosed with and treated for tenosynovial or intra-articular AMIs of the upper extremity distal to and including the elbow. Institutional review board approval was obtained from both centers. Cases of probable AMI without diagnostic culture, cutaneous AMIs, and cases of AMI with follow-up visits of less than 1 year from index surgery were excluded. Only culture-positive cases of tenosynovial or articular infection were included for further study.

Confirmed cases were examined for evidence of aquatic exposure, penetrating trauma, immunosuppressive medications, or comorbidities placing them at an increased risk of acquiring an invasive AMI. Clinical, radiographic, treatment, and outcome data were also obtained.

Comorbidities included organ transplantation, systemic lupus erythematous, rheumatoid arthritis, inflammatory bowel disease, human immunodeficiency virus, active cancer, CREST syndrome, auto-immune hepatitis, previous pulmonary mycobacterial infection, and immunosuppressive medications. Any history of penetrating trauma of any sort was noted. Radiographs were examined for evidence of disease at infection site including soft tissue swelling and articular or bone loss destruction.

Index surgery was defined as the first surgical operation performed following date of presentation. Time to diagnosis was defined as the time from onset until final diagnosis by tissue culture. Subsequent surgeries were defined as all surgical operations related to the AMI following the index surgery.

Treatment outcomes were defined as improved if there was no evidence of residual disability after cessation of therapy and failed if disability persisted, amputation was required, or there was recurrence of infection.

Fisher's exact test was used to compare groups of categorical variables. Welch's unpaired t test was used to compare continuous variables. P<.10 was considered statistically significant.

Results

Thirty-one patients with AMIs were identified who met inclusion criteria. Of these 31 patients, 20 (65%) failed treatment. Seventeen patients were male and 14 were female (Table 1). Mycobacterium marinum was the most frequent organism and accounted for 11 (35%) of the AMIs (Table 2). Mycobacterium marinum infection was associated with aquatic exposure (P=.0002). Four (44%) of the patients with aquatic exposure failed treatment, while 16 (65%) of the patients without aquatic exposure failed treatment. There was no significant association between these groups (P=.2175).

Summary of Clinical Characteristics of 31 Patients With Atypical Mycobacterial Infections

Table 1:

Summary of Clinical Characteristics of 31 Patients With Atypical Mycobacterial Infections

Organisms Causing Atypical Mycobacterial Infection

Table 2:

Organisms Causing Atypical Mycobacterial Infection

Fifteen patients had 1 or more comorbidities, 7 patients had 1 comorbidity, 4 patients had 2 comorbidities, and 4 patients had 3 or more comorbidities. Eight (67%) of the patients with comorbidities failed treatment, although there was no statistically significant association between these groups.

Thirteen patients reported penetrating trauma. Gardening or thorn puncture accounted for 6, wood puncture for 3, boating or fishing for 2, and intravenous drug use for 2. Twelve (80%) of these patients failed treatment compared with 8 (50%) without penetrating trauma. Although insignificant (P=.1315), the observed difference in failure rates between these 2 groups was substantial.

Nine patients had an articular infection, while 22 had a tenosynovial infection (Figure 1). Eight (89%) of the patients with articular infections failed treatment, while 12 (55%) of the patients with tenosynovial infections failed treatment. The observed difference in failure rates between these 2 groups was substantial, but these results were insignificant.

A 58-year-old intravenous opioid abuser presented with a 7-day history of right dorsal hand pain, swelling, erythema, and tenderness to palpation that extended to the distal forearm without fluctuance and with sensation and perfusion intact.

Figure 1:

A 58-year-old intravenous opioid abuser presented with a 7-day history of right dorsal hand pain, swelling, erythema, and tenderness to palpation that extended to the distal forearm without fluctuance and with sensation and perfusion intact.

Three patients showed radiographic evidence of osteomyelitis. All 3 of these patients failed treatment.

Twenty-eight (90%) patients received empiric treatment for their upper extremity infection. Ten patients were treated with antibiotics alone prior to diagnosis, 7 with corticosteroid injection alone, 8 with a combination of antibiotics and corticosteroid injections, 1 with antifungal medication, and 1 with antiparasitic medication. One patient's treatment was unknown, and 3 patients did not receive empiric treatment. All 31 patients eventually received combination antibiotic and surgical treatment after the diagnosis of AMI was determined. Patients saw an average of 5 (range, 2–8) physicians before receiving the correct diagnosis. The average time to diagnosis was 10 months (range, 1–48 months), and the average duration of antibiotic treatment was 10 months (range, 3–40 months). Eleven (73%) of the 15 patients who received corticosteroid injection failed treatment, compared with 56% of those treated without corticosteroid injection. The numbers were too small to show a significant association between these groups (P=.4578).

The most common index surgical procedure was a tenosynovectomy (19 patients). Other index surgeries included incision and drainage (n=7), synovectomy (n=6), carpal tunnel release (n=4), trigger finger release (n=2), removal of nodules (n=2), and removal of foreign body (n=1) (Figures 23). Some index surgeries involved multiple surgical procedures.

The extensor retinaculum was divided and reflected ulnarly. Note extensive tenosynovitis around tendons of the fourth dorsal compartment distal to the retinaculum.

Figure 2:

The extensor retinaculum was divided and reflected ulnarly. Note extensive tenosynovitis around tendons of the fourth dorsal compartment distal to the retinaculum.

Index surgery after debridement: incision and drainage. Intraoperative findings included a white/tan gelatinous material encasing extensor compartments 2 to 5 extending proximal to the extensor retinaculum and tendons intact without fraying. Cultures grew Mycobacterium fortuitum.

Figure 3:

Index surgery after debridement: incision and drainage. Intraoperative findings included a white/tan gelatinous material encasing extensor compartments 2 to 5 extending proximal to the extensor retinaculum and tendons intact without fraying. Cultures grew Mycobacterium fortuitum.

Of the 6 cases of M avium infection, 5 (83%) cases had failure (Figure 4). All 3 (100%) of the infections with M fortuitum led to failure. Mycobacterium avium and M fortuitum led to more failures than any other organism (P=.0133).

Radical debridement of extensor compartments 2 to 5 with extensor carpi radialis brevis sparing 10 weeks after index surgery due to persistent drainage and exposed tendon along distal incision with inability to extend middle and ring fingers.

Figure 4:

Radical debridement of extensor compartments 2 to 5 with extensor carpi radialis brevis sparing 10 weeks after index surgery due to persistent drainage and exposed tendon along distal incision with inability to extend middle and ring fingers.

Discussion

This retrospective case and literature review supports the notion that AMIs of upper extremity synovial-lined structures are underreported despite increasing incidence.3 Diagnosis requires a strong clinical suspicion, and delay in diagnosis can often lead to progression and further invasion of the infection.3,4,13,14 Furthermore, misdiagnosis occurs frequently and can lead to inappropriate management such as corticosteroid injections that exacerbate the infection.15–17 Establishing a diagnosis can be difficult, but there are clues that can guide the surgeon to make the correct diagnosis.

Exposure to aquatic environments, especially with a positive history of puncture wound, is classic for M marinum infection.6,15 Physicians should not assume that joint or tenosynovial swelling following a penetrating injury is noninfectious. One's suspicion should be raised when the swelling is indolent and slowly progressive and there is minimal erythema and tenderness on physical examination. Evidence of granulomatous inflammation on histopathology or culture-positive disease can also lead to diagnosis.15,16 Once a diagnosis has been established, the gold standard for treatment includes surgical intervention followed by long-term antibiotic therapy.10,13,15,18 Although no standard protocol exists for antibiotic choice or treatment duration, AMIs are traditionally treated for 9 months with appropriate antibiotic therapy.3,8–12 The combination of rifampin and ethambutol can be used as empiric treatment until in vitro susceptibility is completed.6,16 The authors propose a management algorithm as shown in Figure 5.

Management algorithm for atypical mycobacterial infections. Abbreviations: AFB, acid-fast bacillus; AMI, atypical mycobacterial infection; ID, infectious disease; mos., months.

Figure 5:

Management algorithm for atypical mycobacterial infections. Abbreviations: AFB, acid-fast bacillus; AMI, atypical mycobacterial infection; ID, infectious disease; mos., months.

In this study, the average length of antibiotic treatment after speciation was 10 months. No significant difference in failure rates was found between cases with shorter or longer diagnosis or antibiotic treatment times. All of the patients were treated with combination surgical intervention and antibiotic therapy.

Corticosteroid treatment is contraindicated with AMIs and is considered inappropriate management.6,15,17 Empiric treatment with corticosteroids leads to delayed wound healing and progression of disease.17,19,20 Although this study did not find a statistically significant increase in morbidity among cases that involved corticosteroid treatment, 73% of these cases had treatment failure compared with 53% of cases that did not receive corticosteroids. To prevent inappropriate management and unsatisfactory outcomes, it is important for physicians to consider a diagnosis of AMI early on in patients with chronic tenosynovitis.6 If a corticosteroid injection is given and the swelling worsens, appropriate biopsy and cultures for acid-fast bacillus, fungus, AMI, and routine aerobic and anaerobic organisms should be performed.

This study had considerably longer time to diagnosis and treatment than that reported in the literature. The mean average delay in diagnosis reported in the literature ranged from 3 to 5 months.15,17,21,22 This study reported an average time to diagnosis of 10 months, with patients consulting an average of 5 physicians prior to receiving a correct diagnosis. As previously mentioned, delay in diagnosis may result in progression of disease, leading to treatment failure and permanent disability. Misdiagnosis on initial presentation is associated with increased time to diagnosis, inappropriate surgical procedures, increased cost, and poor outcomes.15,17

Mycobacterium marinum was the most common atypical mycobacterial organism identified in this study. This atypical mycobacterium is generally associated with aquatic environments, which this study confirmed.2,3 This study also found that significantly more failures occurred with M avium and M fortuitum infections, both of which are strains of rapidly growing mycobacteria.3Mycobacterium avium infections have historically been observed in the setting of human immunodeficiency virus, and recent literature endorses a decline in these infections since the introduction of antiretroviral therapy.23,24 However, other comorbid conditions causing individuals to become immunocompromised have been recognized as predisposing factors for the development of musculoskeletal M avium infections.23,25Mycobacterium avium infection in the setting of immunodeficiency often causes treatment failure and progression to disseminated disease.3 Surgical site infections with M fortuitum, an even rarer infectious organism affecting immunocompromised individuals, have been well documented in the literature.26–28 These postsurgical wound infections may lie dormant for months before becoming clinically apparent.26

Radiographic evidence of disease is not commonly appreciated with AMIs, although bony erosions may be found on magnetic resonance imaging in cases of invasive disease or osteomyelitis.17,23 Approximately 10% of the patients in this study showed radiographic evidence of disease, and all of them failed treatment. This suggests that a high index of suspicion combined with remarkable radiographic evidence may identify aggressive infection and poor prognosis.

This study found an 89% failure rate among articular infections compared with a 55% failure rate among tenosynovial infections. Furthermore, a higher failure rate was observed in patients with penetrating trauma (80%) compared with those without penetrating trauma (50%). These observations suggest that articular infections have an increase in morbidity compared with those of tenosynovial origins, and that infections associated with penetrating trauma have a worse prognosis. These trends are novel with respect to the literature on AMIs; however, they did not prove to be statistically significant, arguably because of low power secondary to small sample.

This study found a 65% failure rate among all cases of upper extremity synovial AMI. This is extraordinarily high when compared with those of other retrospective case series in the literature, which boast failure rates of only 0% to 34%.14–17,19,21,22,25,29,30 This suggests that these infections persist despite adequate treatment and lead to significant morbidity, although the extraordinarily long time needed to make a diagnosis in this study could have caused the higher failure rate.

The hand and wrist are the most common sites of extrapulmonary AMI.2,3 Given such a high failure rate and the predilection toward the upper extremity, it is imperative that physicians maintain a high index of suspicion when evaluating upper extremity synovitis and consider culture for atypical mycobacteria in addition to staining for acid-fast bacteria.5 Lack of awareness, delay in diagnosis, and inappropriate management all can cause complications and lead to permanent disability.

There were several limitations to this study. First, it was difficult to assess how closely the treatment protocol was followed among study participants. Second, surgical interventions were performed by several different surgeons across 2 different health systems. Although this was common among other studies of this nature, a universally agreed on treatment protocol must be developed when handling these infections. More research is needed to elucidate the best protocol for treating AMIs. Finally, the major limitation of this study was lack of power secondary to small sample. Atypical mycobacterial infections are rare, and the study criteria were strict to exclude questionable diagnoses and cases lost to follow-up. Many of the associations and trends observed in this study failed to show statistical significance despite striking differences in outcomes.

Conclusion

Atypical mycobacterial infections should always be considered in the differential diagnosis for infectious etiology of synovial-lined structures. Delay in diagnosis and inappropriate management of these infections may lead to a treatment failure rate that is higher than what has been reported in the literature. M avium and M fortuitum had significantly higher failure rates than other atypical mycobacterial organisms. Articular AMIs and AMIs associated with penetrating trauma tend to cause increased morbidity. A high index of suspicion is required to make a diagnosis and prevent residual disability.

References

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Summary of Clinical Characteristics of 31 Patients With Atypical Mycobacterial Infections

CharacteristicValue
Sex, No.
  Male17
  Female14
Aquatic exposure, No.9
Comorbidities, No.
  17
  24
  3+4
Penetrating trauma, No.
  Gardening/thorn puncture6
  Wood puncture3
  Boating/fishing2
  Intravenous drug user2
Location of injury, No.
  Articular9
  Tenosynovial22
Radiographic evidence of disease, No.3
Treatment prior to diagnosis, No.
  Antibiotics alone10
  Corticosteroid injection alone7
  Combination antibiotics and corticosteroid injection8
  Antifungal1
  Antiparasitic1
Physicians seen prior to diagnosis, No.5
Index surgery, No.
  Removal of foreign body1
  Removal of nodules2
  Incision and drainage7
  Trigger finger release2
  Carpal tunnel release4
  Synovectomy6
  Tenosynovectomy19
Time to diagnosis, average, mo10
Antibiotic time course, average, mo10

Organisms Causing Atypical Mycobacterial Infection

OrganismNo. of Infections
Mycobacterium marinum11
Mycobacterium chelonae6
Mycobacterium avium6
Mycobacterium fortuitum3
Mycobacterium abscessus1
Mycobacterium haemophilum1
Mycobacterium kansasii1
Mycobacterium nonchromogenicum1
Mycobacterium szulgai1
Authors

The authors are from the University of Cincinnati College of Medicine (KPS), the Department of Orthopedic Surgery (PJS), University of Cincinnati Medical Center, and the Department of Orthopedic Surgery (TRK), TriHealth Hand Surgery Center, Cincinnati, Ohio.

The authors have no relevant financial relationships to disclose.

The authors thank Dr Yury Gonzales for technical assistance, Dr Amanda Schroeder for general supervision, and the physicians who performed the surgeries.

Correspondence should be addressed to: Kevin P. Smidt, BS, University of Cincinnati College of Medicine, 557 Ludlow Ave, Cincinnati, OH 45220 ( smidtkp@mail.uc.edu).

Received: August 24, 2017
Accepted: January 22, 2018

10.3928/01477447-20180320-06

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