Ahead of Print -Epidemiology of Human Mycobacterium bovis Disease, California, USA, 2003–2011 - Volume 21, Number 3—March 2015 - Emerging Infectious Disease journal - CDC

full-text ►

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

On This Page

• Medscape CME Activity
• Methods
• Results
• Discussion
• Suggested Citation

Figures

• Figure 1
• Figure 2
• Figure 3

Tables

• Table 1
• Table 2
• Table 3

Downloads

• RIS[TXT - 2 KB]

Mark Gallivan , Neha Shah, and Jennifer Flood

Author affiliations: California Department of Public Health, Richmond, California, USA (M. Gallivan, N. Shah, J. Flood); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (N. Shah)

Suggested citation for this article

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).

References

1. LoBue PA, Enarson DA, Thoen CO. Tuberculosis in humans and animals: an overview. Int J Tuberc Lung Dis. 2010;14:1075–8.PubMed
2. Grange JM. Mycobacterium bovis infection in human beings. Tuberculosis (Edinb). 2001;81:71–7 and. DOIPubMed
3. Sunder S, Lanotte P, Godreuil S, Martin C, Boschiroli ML, Besnier JM. Human-to-human transmission of tuberculosis caused by Mycobacterium bovisin immunocompetent patients. J Clin Microbiol. 2009;47:1249–51 . DOIPubMed
4. Yates MD, Grange JM. Incidence and nature of human tuberculosis due to bovine tubercle bacilli in South-East England: 1977–1987. Epidemiol Infect. 1988;101:225–9. DOIPubMed
5. Majoor CJ, Magis-Escurra C, van Ingen J, Boeree MJ, van Soolingen D. Epidemiology of Mycobacterium bovis disease in humans, the Netherlands, 1993−2007. Emerg Infect Dis. 2011;17:457–63. DOIPubMed
6. LoBue PA, Betacourt W, Peter C, Moser KS. Epidemiology of Mycobacterium bovis disease in San Diego County, 1994–2000. Int J Tuberc Lung Dis.2003;7:180–5 .PubMed
7. Hlavsa MC, Moonan PK, Cowan LS, Navin TR, Kammerer JS, Morlock GP, Human tuberculosis due to Mycobacterium bovis in the United States, 1995–2005. Clin Infect Dis. 2008;47:168–75. DOIPubMed
8. Rodwell TC, Moore M, Moser KS, Brodine SK, Strathdee SA. Tuberculosis from Mycobacterium bovis in binational communities, United States.Emerg Infect Dis. 2008;14:909–16. DOIPubMed
9. Dankner WM, Davis CE. Mycobacterium bovis as a significant cause of tuberculosis in children residing along the United States–Mexico border in the Baja California region. Pediatrics. 2000;105:E79. DOIPubMed
10. Garfein RS, Burgos JL, Rodriquez-Lainz A, Brodine S, Pietrucha A, Rondinelli A, Latent tuberculosis infection in a migrant agricultural community in Baja California, Mexico. J Immigr Minor Health. 2011;13:940–7. DOIPubMed
11. Besser RE, Pakiz B, Schulte JM, Alvarado S, Zell ER, Kenyon TA, Risk factors for positive Mantoux tuberculin skin tests in children in San Diego, California: evidence for boosting and possible foodborne transmission. Pediatrics. 2001;108:305–10. DOIPubMed
12. Center for Disease Control and Prevention. Human tuberculosis caused by Mycobacterium bovis—New York City, 2001–2004. MMWR Morb Mortal Wkly Rep. 2005;54:605–8 .PubMed
13. Ramos DF, Tavares L, Almeida da Silva PE. Molecular typing of Mycobacterium bovis isolates: a review. Braz J Microbiol. 2014;45:365–72.DOIPubMed
14. Ohkusa Y, Shigematsu M, Taniguchi K, Okabe N. Notice to readers: new CDC program for rapid genotyping of Mycobacterium tuberculosis isolates.MMWR Morb Mortal Wkly Rep. 2005;54(Suppl):47–52.PubMed
15. Kurbatova EV, Cavanaugh JS, Dalton T, Click S, Cegielski JP. Epidemiology of pyrazinamide-resistant tuberculosis in the United States, 1999–2009.Clin Infect Dis. 2013;57:1081–93. DOIPubMed
16. de Jong BC, Onipede A, Pym AS, Gagneux S, Aga RS, DeRiemer K, Does resistance to pyrazinamide accurately indicate the presence ofMycobacterium bovis? J Clin Microbiol. 2005;43:3530–2. DOIPubMed
17. Park D, Qin H, Jain S, Preziosi M, Minuto JJ, Mathews WC, Tuberculosis due to Mycobacterium bovis in patients coinfected with human immunodeficiency virus. Clin Infect Dis. 2010;51:1343–6. DOIPubMed
18. Majoor CJ, Magis-Escurra C. van IJ, Boeree MJ, van SD. Epidemiology of Mycobacterium bovis disease in humans, the Netherlands, 1993–2007.Emerg Infect Dis. 2011;17:457–63. DOIPubMed
19. LoBue PA, Moser KS. Treatment of Mycobacterium bovis infected tuberculosis patients: San Diego County, California, United States, 1994–2003.Int J Tuberc Lung Dis. 2005;9:333–8 .PubMed
20. Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35:907–14 .PubMed
21. United States Census Bureau. Population estimates; current estimate data [cited 2014 April 29]. http://www.census.gov/popest/data/index.htm
22. Rodwell TC, Kapasi AJ, Moore M, Milian-Suazo F, Harris B, Guerrero LP, Tracing the origins of Mycobacterium bovis tuberculosis in humans in the USA to cattle in Mexico using spoligotyping. Int J Infect Dis. 2010;14(Suppl 3):e129–35. DOIPubMed
23. Kinde H, Mikolon A, Rodriguez-Lainz A, Adams C, Walker RL, Cernek-Hoskins S, Recovery of salmonella, Listeria monocytogenes, andMycobacterium bovis from cheese entering the United States through a noncommercial land port of entry. J Food Prot. 2007;70:47–52 .PubMed
24. Code of Federal Regulations. Title 9—animals and animal products [9 CFR]. Animal and Plant Health Inspection Service, Department of Agriculture. Subchapter D—exportation and importation of animals (including poultry) and animal products. Part 93—importation of certain animals, birds, fish, and poultry, and certain animal, bird, and poultry products; requirements for means of conveyance and shipping containers [9 CFR 93]. Subpart D— ruminants; Mexico 9, 93.427–93.429; 2000 Jan 1 [cited 2014 April 29]. http://www.gpo.gov/fdsys/granule/CFR-2000-title9-vol1/CFR-2000-title9-vol1-sec93-427
25. Palmer MV, Waters WR. Bovine tuberculosis and the establishment of an eradication program in the United States: role of veterinarians. Vet Med Int. 2011;2011:816345. PMID: 21647341
26. Walker TM, Ip CL, Harrel RH, Evans JT, Kapatai G, Dedicoat MJ, Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis. 2013;13:137–46. DOIPubMed
27. de Kantor IN, LoBue PA, Thoen CO. Human tuberculosis caused by Mycobacterium bovis in the United States, Latin America and the Caribbean. Int J Tuberc Lung Dis. 2010;14:1369–73 .PubMed
28. LoBue PA, LeClair JJ, Moser KS. Contact investigation for cases of pulmonary Mycobacterium bovis. Int J Tuberc Lung Dis.2004;8:868–72.PubMed
29. Lighter J, Rigaud M. Diagnosing childhood tuberculosis: traditional and innovative modalities. Curr Probl Pediatr Adolesc Health Care.2009;39:61–88. DOIPubMed
30. Andersen P, Doherty TM. The success and failure of BCG - implications for a novel tuberculosis vaccine. Nat Rev Microbiol. 2005;3:656–62.DOIPubMed
31. Fine PE. Variation in protection by BCG: implications of and for heterologous immunity. Lancet. 1995;346:1339–45. DOIPubMed
32. García-Rodríguez JF, Álvarez-Díaz H, Lorenzo-García MV, Mariño-Callejo A, Fernandez-Rial Á, Sesma-Sánchez P. Extrapulmonary tuberculosis: epidemiology and risk factors. Enferm Infecc Microbiol Clin. 2011;29:502–9. DOIPubMed
33. Colditz GA, Berkey CS, Mosteller F, Brewer TF, Wilson ME, Burdick E, The efficacy of bacillus Calmette-Guerin vaccination of newborns and infants in the prevention of tuberculosis: meta-analyses of the published literature. Pediatrics. 1995;96:29–35 .PubMed

Figures

• Figure 1. Number of verified tuberculosis case-patients eligible for inclusion in an epidemiologic study of human Mycobacterium bovis disease, California, USA, 2003–2011.
• Figure 2. Cumulative incidence of human Mycobacterium bovis disease, by region, California, USA, 2003–2011.
• Figure 3. Annual number of case-patients with Mycobacterium bovis disease and percentage of tuberculosis cases attributable to M. bovis, California, USA, 2003–2011.

Tables

• Table 1. Sociodemographic and clinical characteristics of and treatment outcomes for case-patients with tuberculosis attributable to Mycobacterium bovis, California, USA, 2003–2011
• Table 2. Sociodemographic and clinical characteristics of and treatment outcomes for case-patients with tuberculosis attributable to Mycobacterium bovis and M. tuberculosis, California, USA, 2003–2011
• Table 3. Multivariate model of sociodemographic and clinical characteristics associated with Mycobacterium bovis disease versus M. tuberculosisdisease, California, USA, 2010–2011

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

DOI: 10.3201/eid2103.141539