Extrapulmonary Nontuberculous Mycobacterial Disease Surveillance — Oregon, 2014–2016

Characteristics of Extrapulmonary NTM Cases

During 2014–2016, a total of 134 extrapulmonary NTM cases were reported in Oregon (11 per 1 million persons per year). Patients ranged in age from 10 months to 92 years (median age = 50.8 years). Seventy (52%) patients were female, 96 (72%) were white, 43 (33%) were hospitalized, 18 (15%) developed sepsis, and one (1%) died. Among patients for whom exposure risk factors were reported, the most frequently reported predisposing factors were soil exposure (41/98; 42%), immunocompromised condition (42/124; 34%), and surgery (32/120; 27%). Approximately two thirds of patients (68%) reported more than one predisposing factor (Table 1). A bimodal age distribution was observed, with highest number of cases and the highest incidence among persons aged 0–9 years (20 per 1 million persons per year) and persons aged 60–69 years (18 per 1 million persons per year) (Table 2). Among 29 infections in patients aged 0–9 years, 25 (86%) were caused by Mycobacterium avium complex. Among 26 infections in patients aged 60–69 years, six (23%) were caused by Mycobacterium avium complex. The remainder of cases in this age group primarily was caused by either M. chelonae or M. abscessus (nine; 35%) or M. fortuitum (six; 23%) (Figure).

Among persons aged 0–9 years, 76% had infected lymph nodes, compared with 4% among persons aged 60–69 years. The latter age group’s most common specimen sources were tissue (31%) (not further specified), wounds (19%), blood (12%), and joints (12%).

Detection and Management of Extrapulmonary NTM Outbreaks

An outbreak of seven M. fortuitum infections in two small neighboring counties was initially reported by hospital staff members after the outbreak had begun in July 2013 and before mandatory reporting had commenced in January 2014. The outbreak was associated with knee and hip replacement procedures during 2013–2014, a single device manufacturer, and multiple hospitals and operating room staff members. The investigation began 102 days after the second confirmed laboratory report became available. Intraoperative risks identified included suboptimal surgical infection control practices. The presence of a single device manufacturer representative^† at six of the seven surgical procedures was associated with NTM surgical site infection. Oregon Health Authority received no reports of cases of M. fortuitum infections among joint replacement patients beyond the two counties. Public health officials recommended that all operating room staff members adhere to the Association of Perioperative Registered Nurses infection control guidelines.

During 2015, two M. haemophilum infections were reported to a local health department; both involved receipt of tattoos at the same tattoo parlor. The outbreak investigation began 33 days after the second confirmed laboratory report became available. The tattoo artist used water from a cooler to dilute ink and wipe tattoos during their placement. After public health officials recommended using sterile water, no additional extrapulmonary NTM infections were associated with the parlor.

Costs of Establishment and Maintenance of Extrapulmonary NTM Surveillance

All estimated costs related to extrapulmonary NTM surveillance were for salaries. Local health department nurses reported spending approximately 90 minutes investigating each case. Incremental direct costs to add extrapulmonary NTM to public health notifiable disease surveillance were approximately $6,000 for implementation and approximately $10,000 in annual operating costs.

Discussion

During 2005–2006, an analysis of Oregon laboratory data reported an annual extrapulmonary NTM infection prevalence of 16 cases per 1 million persons (1); however, clinical data were insufficient to characterize disease burden, and the authors reported only prevalence, not incidence data. In January 2014, extrapulmonary NTM infections became reportable in Oregon. Although extrapulmonary NTM infections are rare, they can be associated with substantial severity, including hospitalization, sepsis, and death. Costs to set up and maintain the surveillance system were minimal. Limited time was needed to investigate each case, case counts were few, and existing electronic reporting infrastructure minimized laboratory reporting costs.

In Oregon, extrapulmonary NTM surveillance detected outbreaks, augmented case finding, and guided subsequent control measures. Surveillance aided the outbreak investigation among joint replacement patients; the lack of cases reported elsewhere in the state argued against widespread product contamination during manufacturing. That is, because NTM was reportable in Oregon, surveillance would have identified extrapulmonary NTM infections among joint replacement patients in other counties if a production site contaminated the products. Surveillance for extrapulmonary NTM infections also detected the outbreak among tattoo parlor patrons who lacked a common health care provider who might have recognized a pattern and reported the outbreak. Time to investigation of the tattoo parlor–associated outbreak was 69 days shorter than the time to investigate the previous outbreak that began before mandatory extrapulmonary NTM reporting. If the outbreak among joint replacement patients had occurred when reporting and surveillance procedures were established, the investigation might have begun sooner.

Detection of extrapulmonary NTM outbreaks can be delayed if the condition is not reportable. For example, NTM is not reportable in Georgia. Investigation of an outbreak of extrapulmonary M. abscessus infections after dental pulpotomy in Georgia commenced approximately 1 year after the second case was diagnosed; 20 cases among children were ultimately identified (8) (Melissa Tobin-D’Angelo, Georgia Department of Public Health, personal communication, June 2018).

It is important for clinicians to be aware of the possibility of an NTM outbreak because they can help identify extrapulmonary NTM outbreaks. In 2013, a clinician reporting two extrapulmonary NTM cases among medical tourists led to detection of an NTM outbreak traced to cosmetic surgery centers in the Dominican Republic; subsequent case finding identified outbreak cases from four other states (9,10). Extrapulmonary NTM surveillance could enhance detection and identification of the source of multijurisdictional outbreaks. Contaminated cardiopulmonary bypass heater-cooler devices have caused a large, ongoing international outbreak of M. chimaera infections among cardiac surgery patients (2). Long incubation periods complicated detection of this outbreak. Systematic extrapulmonary NTM surveillance in other states and countries might have led to earlier detection.

The findings in this report are subject to at least three limitations. First, the routinely asked predisposing factor questions did not specify whether a particular factor (e.g., surgery) involved the infection site, which could have resulted in overestimates of that factor’s impact. In January 2018, the case report form was revised to address this issue. Second, sensitivity of extrapulmonary NTM surveillance might be limited because clinicians might not suspect extrapulmonary NTM infection and, consequently, might not order cultures for mycobacteria. Finally, these data only represent cases diagnosed in Oregon during 2014–2016 and are not generalizable to other states because of different population characteristics, predisposing factor rates, and adoption of electronic laboratory reporting.

To promote nationwide extrapulmonary NTM surveillance, CSTE developed a standardized case definition for extrapulmonary NTM surveillance (6). State and territorial public health authorities can use this case definition to ensure compatible surveillance across jurisdictions. In addition, the Oregon Health Authority improved its investigative guidelines and case report form by making the predisposing factor questions body-site specific. Forms are publicly available for states and territories to adapt for extrapulmonary NTM surveillance implementation (7). NTM surveillance is ongoing in Oregon.

Extrapulmonary NTM infections cause considerable morbidity, sometimes resulting in hospitalization or sepsis, in Oregon. Systematic reporting of these infections has led to detection and control of outbreaks at relatively low cost. Publicly available resources (e.g., the CSTE case definition, Oregon’s investigative guidelines, and the Oregon case report form) offer states and territories adaptable tools to implement extrapulmonary NTM surveillance.