Ahead of Print -Epidemiology of Human Mycobacterium bovis Disease, California, USA, 2003–2011 - Volume 21, Number 3—March 2015 - Emerging Infectious Disease journal - CDC
Volume 21, Number 3—March 2015
CME ACTIVITY - Research
Epidemiology of Human Mycobacterium bovis Disease, California, USA, 2003–2011
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Abstract
We conducted a retrospective review of California tuberculosis (TB) registry and genotyping data to evaluate trends, analyze epidemiologic differences between adult and child case-patients withMycobacterium bovis disease, and identify risk factors for M. bovis disease. The percentage of TB cases attributable to M. bovis increased from 3.4% (80/2,384) in 2003 to 5.4% (98/1,808) in 2011 (p = 0.002). All (6/6) child case-patients with M. bovis disease during 2010–2011 had >1 parent/guardian who was born in Mexico, compared with 38% (22/58) of child case-patients with M. tuberculosis disease (p = 0.005). Multivariate analysis of TB case-patients showed Hispanic ethnicity, extrapulmonary disease, diabetes, and immunosuppressive conditions, excluding HIV co-infection, were independently associated with M. bovisdisease. Prevention efforts should focus on Hispanic binational families and adults with immunosuppressive conditions. Collection of additional risk factors in the national TB surveillance system and expansion of whole-genome sequencing should be considered.
Mycobacterium bovis, part of the Mycobacterium tuberculosis complex, is a zoonotic pathogen that can cause tuberculosis (TB) disease in a broad range of mammalian hosts (1). TB disease caused by M. bovis is clinically, radiographically, and pathologically indistinguishable from TB caused by M. tuberculosis (2). M. bovistransmission to humans most frequently occurs through consumption of unpasteurized, contaminated dairy products, but person-to-person transmission has been reported (3,4). The consumption of contaminated unpasteurized dairy products has been suggested as a major contributor to human M. bovis disease for several reasons: 1) the near absence of M. bovis disease among infants <12 months of age; 2) a high percentage of extrapulmonary disease, particularly abdominal disease, among patients with M. bovis disease; and 3) an association between positive interferon-γ release assay results and consumption of unpasteurized dairy products (5–11).
In the United States, 1%–2% of all human TB cases are attributable to M. bovis infection (7), but in certain geographic regions and communities, human M. bovis infection accounts for a much higher percentage of the cases. During 2001–2005, M. bovis accounted for nearly 10% of culture-positive TB isolates in San Diego, California, USA, including 54% of those from children (<15 years of age) and 8% of those from adults (>15 years of age) (8). Nearly all (97%) case-patients with M. bovis disease were among the Hispanic population, and 60% of those case-patients were born in Mexico (8). During 2001–2004, an investigation in New York, New York, USA, showed a high prevalence of TB caused by M. bovis among the Hispanic community. New York investigators reported that 57% of M. bovis case-patients were born in Mexico, and 83% of the interviewed case-patients consumed unpasteurized cheeses produced in Mexico while living in the United States (12).
The internationally recognized genotypic method for identifying M. bovis is spacer oligonucleotide typing (13). In 2004, the CDC (Centers for Disease Control and Prevention) Tuberculosis Genotyping Program (now called the National Tuberculosis Genotyping Service,http://www.cdc.gov/tb/publications/factsheets/statistics/genotyping.htm) began spoligotyping M. tuberculosis complex isolates from US patients with culture-positive TB (14). In California, the percentage of culture-positive isolates spoligotyped each year has gradually increased from 35% in 2004 to 92% in 2011. The incompleteness and variability (by geographic location) of spoligotype testing over this period exclude trend analysis and population-basedM. bovis studies using this genotypic method. However, pyrazinamide monoresistance can serve as a proxy measure for M. bovis because M. bovis is intrinsically resistant to pyrazinamide but pyrazinamide monoresistance is rare among M. tuberculosis isolates (7,15,16). A recent national study on pyrazinamide resistance showed that 0.7% (196/27,428) M. tuberculosis isolates were pyrazinamide monoresistant (15). Since 2003, ≈97% of all culture-positive TB isolates in California have had initial (i.e., pretreatment) drug susceptibility testing for pyrazinamide, isoniazid, and rifampin.
M. bovis disease is of particular concern because of the high percentage of cases among children and because of its association with zoonotic and foodborne transmission, HIV co-infection, and poor treatment outcomes compared with M. tuberculosis disease (6,17–19). Further investigation into M. bovis disease is needed to understand the epidemiology of cases among children and adults, its association with immunosuppressive conditions, and the association of those conditions with treatment outcomes. We conducted a retrospective review of California TB surveillance data to evaluate trends for TB cases attributable to M. bovis, evaluate epidemiologic differences between M. bovis TB cases in adults and children, and identify risk factors associated with M. bovis disease compared with M. tuberculosis disease. We also conducted an evaluation of the accuracy of pyrazinamide monoresistance as a proxy measure for M. bovis disease by using surveillance and genotyping data.
Mr. Gallivan is an epidemiologist in the Immunization Branch, California Department of Public Health. His research interests include TB infection treatment strategies, public health practice, and vaccine-preventable disease epidemiology.
Acknowledgments
We acknowledge the efforts of local health departments and laboratories in California who collected and reported the data used in this study.
This project was supported in part by the appointment of M.G. to the Applied Epidemiology Fellowship Program administered by the Council of State and Territorial Epidemiologists and by funding from CDC (cooperative agreement no. 1U38HM000414).
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Suggested citation for this article: Gallivan M, Shah N, Flood J. Epidemiology of human Mycobacterium bovis disease, California, USA, 2003–2011. Emerg Infect Dis. 2015 Mar [date cited]. http://dx.doi.org/10.3201/eid2103.141539
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