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No. 3, 2005
Mycobacterium bovis in New
York City—an Unexpected TB Investigation
A full description of the investigation of human M. bovis infection
in New York City was published in the MMWR: CDC. Human
tuberculosis caused by Mycobacterium bovis—New York City, 2001–2004.
MMWR 2005 June 24; 54(24): 605-608.
Background. In January 2001, the New York City Department of Health
and Mental Hygiene (DOHMH) Bureau of TB Control (BTBC) began genotyping
isolates from all culture-positive TB cases using two methods, IS6110-based
restriction fragment length polymorphism (RFLP) and spoligotyping.
A protocol was developed for conducting cluster investigations when
two or more isolates shared the same RFLP and spoligotype, with
the goal of identifying previously unrecognized epidemiological
links between the cases.
In February 2002, a cluster of three cases of TB due to the same
strain of Mycobacterium bovis (M. bovis) was detected,
and a cluster investigation was initiated. Over the next 18 months,
several more cases sharing the same spoligotype were detected, as
were additional clusters of M. bovis with different spoligotypes.
No human-to-human transmission linkages were established within
any of the clusters, but two significant observations were made.
First, it was noted that the patients were mostly Mexico-born, many
from the Puebla region of Mexico.
Second, several US-born children were included in the largest cluster
of M. bovis cases, all of Mexico-born parents.
In September 2004, a case of fatal peritonitis due to M. bovis
in a 15-month-old child came to the attention of the Director of
the BTBC. The case highlighted the question that had been asked
but not yet answered during the cluster investigations, “Why would
a US-born child have TB due to M. bovis?” Even before universal
genotyping in NYC, M. bovis was the presumed source of infection
for a handful of pyrazinamide-resistant patients each year; however,
the cases occurred in non–US-born adults from countries where bovine
TB and unpasteurized dairy products were prevalent, and the disease
was regarded as reactivation of latent infection acquired outside
of the United States.
The US-born children with TB due to M. bovis challenged
our typical thinking about the source of this infection. Were the
children traveling out of NYC and becoming infected in the country
of birth of their parents, Mexico?
Were the children exposed to infectious pulmonary cases of TB due
to M. bovis in NYC? Was there a foodborne source of infection
in NYC, as investigators in San Diego postulated for their pediatric
TB cases? In San Diego, health officials attributed pediatric TB
due to M. bovis to the readily available unpasteurized Mexican
cheese across the border, but transborder traffic could not as easily
account for M. bovis in NYC.
In addition to the usual source-case investigations conducted
for all pediatric TB cases and the cluster investigations underway
based on genotyping, we re-interviewed all available patients (or
parents of patients) to try to identify the source of M. bovis
infection. We also began an investigation into foodborne transmission,
an endeavor which was new to the usual scope of work of the BTBC.
With the assistance of staff of DTBE and the National Center for
Infectious Diseases (NCID), we developed contacts within the US
Food and Drug Administration (FDA) and the US Department of Agriculture
(USDA). In addition, we partnered with the NYC DOHMH Bureau of Communicable
Diseases and the New York State Department of Agriculture and Markets
(NYS Ag and Markets). Finally, we sought laboratories best able
to test samples of Mexican cheese for the presence of M. bovis.
Through our interviews, we learned that most of the US-born
children had never traveled outside of the country, and had no history
of exposure to the few pulmonary TB cases due to M. bovis
that had occurred in New York City. We also found that many of our
patients had consumed Mexican-produced cheeses while living in New
York City. They had obtained these products from friends or family
who had transported it in luggage, through courier agencies, from
Mexican grocers, and from door-to-door vendors.
From the USDA and the NYS Ag and Markets, we learned that cattle
in New York State and surrounding states are certified “TB-free”
and that dairy products sold in retail stores in New York State
must be pasteurized. Also from the USDA, we learned that couriers
arriving from Mexico with
packages intended for individual consumption may bring dairy items
into the United States,
but are prohibited from bringing in produce, chicken, and pork.
Though couriers ostensibly bring packages into the country for individual
consumption, they may bring large quantities of food that has the
potential to be sold commercially. From the FDA, we learned that
cheeses imported for retail sale must be pasteurized unless aged
greater than 60 days. We also learned that imports of soft cheeses
arrive daily in the United States
and that most of these imports are not inspected owing to lack of
Our search for a laboratory that would work with us led us beyond
the mycobacteria lab we were familiar with. We learned that laboratories
must have a Biosafety Level 3 certification to attempt to isolate
this organism from food. This excluded the FDA laboratory. The NYC
TB lab, though familiar with mycobacteria, did not work with food
products. The DOHMH environmental lab was willing to attempt to
grow the organism from cheese, but was more familiar with common
foodborne bacteria and less familiar with the properties associated
with mycobacteria. They developed a protocol for testing cheese
samples but have not had success at growing the organism to date.
The USDA laboratory in Ames, Iowa, was experienced in working with
this organism through efforts in bovine TB eradication in Texas,
New Mexico, Michigan, and California, and they were willing to work
with us. The Ames laboratory agreed to develop a protocol for testing
cheese samples for the presence of the M. bovis, and also
for comparing the genotyping of our human cases with bovine cases
in the Ames database.
While we knew that human TB due to M. bovis was not uncommon
in regions of the world where dairy pasteurization is not universal
and bovine TB remains problematic, we did not expect to find it
in US-born children in New York City. We were not familiar with
investigating foodborne transmission, and we had to adapt what we
learned from investigations of other foodborne pathogens such as
Listeria monocytogenes and Salmonella sp. to M.
bovis which has a potential latency far in excess of these organisms.
We have learned that within a certain subset of our population,
the Mexican community, it is not difficult to obtain food items
that are produced outside of the United States and that may not
meet federal and state standards for food safety. We have had to
review and revise the materials available to providers and to the
public regarding TB disease to include the possibility of foodborne
transmission of TB.
The investigation of M. bovis in New York City is ongoing.
We continue universal genotyping of isolates of all culture-positive
TB cases. We are collaborating with the USDA laboratory in comparing
human M. bovis isolates with M. bovis isolates from
cattle in the United States
and Mexico, and in testing
of cheeses obtained in New York City and produced in Mexico.
We have partnered with Mexican community groups and are disseminating
information about M. bovis to the community. In addition,
we are planning to investigate the prevalence of latent TB infection
among US-born children of Mexican parents and the prevalence of
consuming Mexican-produced cheeses among these children.
Though we did not anticipate a foodborne-transmission investigation
as part of our mandate in TB control, the M. bovis investigation
has alerted us to a mode of TB transmission that is rare overall
in industrialized nations, but is significant within certain segments
of our population.
—Submitted by Ann Winters, MD,
Michelle Macaraig, MPH,
Carla Clark, MPH, Cynthia Driver, DrPH,
Sonal Munsiff, MD, and Carolina
New York City Department of Health and Mental Hygiene, Bureau
of TB Control
Dr. Munsiff is also affiliated with DTBE