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Epidemiology of Tuberculosis in the United States


									                                            Clin Chest Med 26 (2005) 183 – 195

         Epidemiology of Tuberculosis in the United States
            Eileen Schneider, MD, MPHa,*, Marisa Moore, MD, MPHa,b,
                              Kenneth G. Castro, MDa
    Division of Tuberculosis and Elimination, Centers for Disease Control and Prevention, 1600 Clifton Road, MS E-10,
                                                 Atlanta, GA 30333, USA
         TB Control Program, San Diego County Health and Human Services, Department of Public Health Services,
                              3851 Rosecrans Street, MS P511D, San Diego, CA 92110, USA

Historical background                                           data collection was a priority for the National Tu-
                                                                berculosis Association. As the mortality rate con-
    The epidemiology of tuberculosis (TB) in the                tinued to decrease, attention focused on TB case
United States has changed remarkably over the last              finding. Armed with a new diagnostic tool, the chest
2 centuries. In the nineteenth century, TB was the              roentgenogram, mass chest radiograph screenings
leading cause of death. As the nineteenth century prog-         were conducted beginning in the early 1930s and
ressed, TB mortality decreased, partly because of               continuing into the 1950s, enabling the diagnosis of
improved socioeconomic conditions [1,2], especially             TB patients before they became symptomatic [2].
in urban settings, and partly owing to the natural                  The need to expand data collection to include TB
behavior of epidemics [3]. After the tubercle bacillus          morbidity in addition to TB mortality was acknowl-
was identified as the causative agent of TB by Robert           edged [1,2]. Reliable and complete morbidity data
Koch in 1882, the approach to TB control changed                would allow TB experts to measure more accurately
greatly, and the concepts of public health, prevention,         the magnitude of the TB problem and the effec-
and segregation of TB patients gained more accep-               tiveness of control efforts. In 1920, the National Tu-
tance. As a result, in industrialized countries, the            berculosis Association published its first Diagnostic
prescribed treatment of rest, isolation, nutrition, and         Standards and Classifications of TB to assist health
fresh air for TB patients was achieved with long stays          care providers and standardize diagnostic criteria
in sanatoria [1,2].                                             [5,6]. National TB mortality and morbidity data,
    By the late 1800s, TB was more than ever con-               coordinated by the National Tuberculosis Associa-
sidered a public health issue, even though there were           tion, became available in 1933. In 1944, a United
few well established local or state public health               States Public Health Service Act mandated the crea-
departments [1,2,4]. More resources became avail-               tion of a national TB control program [1]. With
able, and public health programs dedicated to TB con-           the introduction of the therapeutic agents streptomy-
trol were established. In 1904, the first voluntary             cin (1947), p-aminosalicylic acid (1949), isoniazid
health agency dedicated to TB, the National Tuber-              (1952), and pyrazinamide (1952) TB mortality rates
culosis Association (now the American Lung Asso-                decreased dramatically. Between 1930 and 1960, the
ciation), was organized [1,5]. TB surveillance and              mortality rate decreased by 92%, from 71 to 6 deaths
                                                                per 100,000 population.
                                                                    Because of the widespread use of chemotherapy,
   This work was funded by the Division of Tuberculosis         long hospitalizations for TB were no longer needed,
and Elimination, Centers for Disease Control and Prevention.    and TB sanatoria and hospitals began to close [1,2,5].
   * Corresponding author.                                      Having a standard definition for a reportable case of
   E-mail address: (E. Schneider).                 TB for surveillance purposes became paramount [7],

0272-5231/05/$ – see front matter. Published by Elsevier Inc.
184                                               schneider et al

and in 1951, a committee consisting of state TB con-        Reporting of RVCT data to the CDC also will
trol officers and sanatoria directors published recom-      be modified with the transitioning of the TIMS to
mendations for TB case reporting and counting               the Web-based National Electronic Disease Surveil-
procedures [8]. In 1952, the United States Public           lance System.
Health Service (USPHS) Tuberculosis Control Pro-
gram instituted procedures to report new cases of
TB. Not until 1953, through the cooperation of the          Tuberculosis resurgence
states, did the USPHS receive reports from the entire
United States, heralding the birth of the national TB           Noting that extraordinary strides against TB have
surveillance system [1,2].                                  been made both in treatment and surveillance since
                                                            the 1950s, many TB experts have believed that TB
National tuberculosis surveillance system                   elimination in the United States is within reach [1,2].
                                                            In 1959, the historic Arden House Conference, spon-
    Since 1953, the national TB surveillance system         sored by the National Tuberculosis Association and
has been modified several times to monitor and re-          the USPHS Tuberculosis Control Program, brought
spond better to changes in TB morbidity. Data are           together TB experts to formulate a plan on how to
collected on TB cases that have been verified and           eliminate TB; this plan served as a basis for future TB
have met the Centers for Disease Control and Pre-           control efforts [12]. TB incidence continued to
vention (CDC) public health surveillance case defi-         decrease. From 1953 through 1985, TB case numbers
nition for TB [9,10]. TB is a reportable disease in         decreased by 74%, from 84,304 to 22,201 cases,
each state [11]. In 1985, the national TB surveillance      and the case rate decreased by 82%, from 53.0 to
system changed: originally collecting aggregate data,       9.3 cases per 100,000 population. As a result, many
the CDC began collecting individual case reports            no longer considered TB to be a major problem.
on a form called the Report of Verified Case of             In the early 1970s, federal funding allocated for
Tuberculosis (RVCT). Currently, data are collected          TB control began to decrease, and, as a result, many
by reporting areas (the 50 states, the District of Co-      TB control services were dismantled [13,14]. Al-
lumbia, New York City, Puerto Rico, and jurisdic-           though TB funds were decreasing, the cost of treating
tions in the Pacific and Caribbean) using the RVCT.         TB was increasing. In 1981, only $3.7 million was
An RVCT is completed for each reported new TB               appropriated to the CDC to fight TB nationally.
disease case and contains patient demographic, clini-           In 1987, the Advisory Committee (now Council)
cal, and laboratory information. An RVCT is com-            for Elimination of Tuberculosis (ACET) was estab-
pleted by the health department for each confirmed          lished, and its membership was directed to develop a
TB case and transmitted to the CDC to be included           strategic plan for TB elimination [15]. The ACET and
in the national TB surveillance database. The CDC           the CDC published this plan, proposing a TB in-
annually publishes a report summarizing national            cidence interim goal for the year 2000 of 3.5 or fewer
TB statistics [10]. Also included in this annual report     TB cases per 100,000 population and an elimination
are the ‘‘Recommendations for Counting Reported             target of less than 1 TB case per million population
TB Cases,’’ which were last revised in 1997.                by 2010. In the mid-to-late 1980s, however, the
    The CDC has maintained a computer database              longstanding downward trend in TB incidence was
on TB surveillance data since 1985. State and local         interrupted. In 1986, a 2.6% annual increase in the
TB programs have been able to collect, manage, and          case number was documented, signaling the begin-
transfer TB surveillance data (i.e., RVCT) electroni-       ning of the TB resurgence (Fig. 1). In the late 1980s,
cally to the CDC first through software for expanded        after decades of decreasing TB incidence, TB once
TB surveillance (SURVS-TB, 1993 – 1997) and cur-            again became a major threat.
rently through the Tuberculosis Information Manage-             The resurgence had a significant impact on TB
ment System (TIMS, 1998 – present). In 1993, the            control strategies in the United States. Because of
RVCT was expanded to collect additional information         newly identified risk groups, the focus of many TB
(eg, drug resistance, HIV infection) in response to the     control strategies had to be shifted, and many pro-
TB epidemic of the mid-to-late 1980s and early              grams needed to be overhauled. CDC researchers
1990s. The most recent modification was imple-              concluded that the resurgence had resulted in an es-
mented in January 2003 to meet federal standards for        timated 52,100 excess TB cases from 1985 through
the classification of race and ethnicity. Additional        1992 [16]. Several factors have been linked to the
changes for the national TB surveillance system are         resurgence, including the deterioration of the TB
on the horizon with a revision of the RVCT.                 program infrastructure, the HIV/AIDS epidemic,
                                                epidemiology of tuberculosis in the united states                                     185


                     Number of TB Cases

                                                    1981 1983 1985 1987 1989 1991 1993 1995 1997 1999 2001 2003

                                          Fig. 1. Reported tuberculosis cases in the United States from 1981 to 2003.

drug-resistant TB, TB among foreign-born persons,                                  veillance, augment case finding and contact inves-
and an increase in transmission, especially in con-                                tigations, advance laboratory capacity (eg, drug-
gregate and institutional settings [16 – 19].                                      susceptibility testing and new diagnostic tools), and
    The degree to which each of these factors affected                             ensure each patient completed therapy through the
TB control at the local level varied, but two of these                             use of directly observed therapy (DOT).
factors, the HIV/AIDS epidemic and TB among
foreign-born persons, strongly influenced the TB re-
surgence in the United States. HIV infection is con-
sidered to be the greatest risk factor known today                                 After the tuberculosis resurgence, 1993 – 2003
for TB. Several large outbreaks of multidrug-resistant
TB (MDR-TB) (ie, TB resistant to at least isoniazid                                    During the resurgence, the national TB incidence
and rifampin) among persons infected with HIV were                                 peaked in 1992 at 26,673 cases (10.5 cases per
documented in Florida and New York City [20 – 22].                                 100,000 population). The aggressive attack on TB in
In 1991, 41% of culture-positive TB patients in New                                the United States resulted in the annual TB case num-
York City were also infected with HIV, and 19% had                                 ber and case rate decreasing in 1993 to 25,108 cases,
MDR-TB [23]. Early diagnosis of TB among persons                                   9.7 cases per 100,000 population. Tuberculosis be-
infected with HIV was difficult because of the lack of                             came more localized to well-defined risk groups and
specific clinical findings, such as a positive tuberculin                          geographic areas [34,35]. In response, strategic plans
skin test result and an abnormal chest radiograph.                                 were revised to help prioritize efforts and outline
Ineffective isolation precautions also contributed to                              updated recommendations for TB elimination in the
nosocomial transmission of MDR-TB among patients                                   United States [36,37].
and health care providers [24 – 26]. HIV-related TB                                    From 1993 to 2002, the average year-to-year de-
outbreaks were also documented in other congregate                                 crease in TB rate was 6.9%. In 2003, however, the
settings [27] such as correctional facilities [28] and                             CDC reported the smallest annual decrease in the TB
homeless shelters [29,30]. Another important factor                                rate (1.9%) and TB case numbers (184) since the re-
fueling the TB resurgence was the immigration of                                   surgence, raising concern about a possible slowing
persons from countries that have high rates of TB                                  of the progress against TB. For 2003, 14,874 TB
[19]. The proportion of reported TB cases among                                    cases were reported in the United States, with a rate
foreign-born persons increased from 22% in 1986                                    of 5.1 per 100,000 population that remains higher
(the first year birthplace data were collected by the                              than the national interim goal of 3.5 cases per
national TB surveillance system) to 30% in 1993.                                   100,000 population set for 2000. Moreover, despite
    In the early 1990s, the newly established Federal                              the decline in TB nationwide, rates have increased
Tuberculosis Task Force revaluated existing TB                                     in certain states, and elevated TB rates continue to be
strategies and formulated the National Action Plan                                 reported in certain populations (eg, foreign-born per-
to Combat MDR-TB [31]. In the United States, a                                     sons and racial/ethnic minorities). In 2003, 12 states
monumental public health effort to control TB was                                  and the District of Columbia reported case rates
initiated [32,33]. Federal funding was increased and                               above the national average, and 20 states reported
used to rebuild the TB infrastructure, strengthen sur-                             increases in case number compared with 2002 [10].
186                                                  schneider et al

Age                                                            portion of foreign-born TB patients remained rela-
                                                               tively stable at 22% to 23% until 1990, when the
    The distribution of TB cases and case rates                proportion and number of cases among foreign-born
among age groups remained relatively stable. In                persons began to increase (Fig. 2). Since then, the
2003, 34.2% of TB patients were 25 to 44 years old,            proportion has increased steadily, with foreign-born
28.9% were 45 to 64, 20.2% were 65 years and                   persons accounting for 53.4% of the national case
older, 10.6% were 15 to 24 years, and 6.2% were                total in 2003. This trend results from the relatively
children under 15 years. In contrast, 2003 TB case             stable case count in foreign-born persons since the
rates (cases per 100,000 population) were highest              mid 1990s, with 7902 cases reported in 2003,
(8.4) among persons 65 years and older, followed by            coupled with the significant decrease in cases among
a rate of 6.3 for those 45 to 64, 6.0 for those 25 to          US-born persons (Fig. 3). In 1992, 19,225 cases
44 years, 3.8 for those 15 to 24 years, and 1.5 for            among US-born persons were reported in the United
children under 15. Although TB case rates among                States; this number decreased to 6903 in 2003.
children under 15 are low, certain groups of children              TB case rates among foreign-born persons have
(eg, younger children, racial and ethnic minorities,           been consistently higher than among US-born per-
and foreign-born children) are at higher risk for TB           sons [40]. The 2003 TB rate among all foreign-born
[38]. Children pose unique challenges to TB control:           persons (23.6 cases per 100,000 population) was
                                                               8.8 times greater than that among US-born persons
      1. TB in children is considered a sentinel event,        (2.7 cases per 100,000 population). Six birth coun-
         usually indicating recent transmission.               tries of foreign-born TB patients have consistently
      2. TB diagnosis in children, especially in children      accounted for approximately 60% of the foreign-
         under 5 years of age, can be more difficult be-       born TB cases reported in the United States annually.
         cause they often have nonspecific signs and           In 2003, Mexico accounted for 25.6% of foreign-
         symptoms and fewer positive bacteriologic             born patients; the Philippines, 11.5%; Viet Nam,
         tests because of the paucity of mycobacteria.         8.4%; India, 7.6%; China 4.8%; and Haiti 3.3%. The
      3. Children, especially infants, are at an increased     number of states reporting 50% or more of their
         risk for progressing from latent TB infection         TB cases among foreign-born persons has also been
         (LTBI) to active and sometimes severe TB dis-         increasing, from two states in 1986, to 14 states in
         ease [38].                                            1998, and to 25 states in 2003 (Fig. 4). Five states
                                                               have consistently reported the most foreign-born
                                                               TB patients: California, New York, Texas, Florida,
                                                               and New Jersey. In 2003, these states combined re-
                                                               ported almost two thirds of the total cases in foreign-
    Disparities in TB rates persist among racial and
                                                               born TB persons (California, 30.6%; New York,
ethnic minority populations (Table 1). Overall, the
                                                               12.4%; Texas, 9.0%; Florida, 5.9%; and New Jersey,
highest TB rates are seen among Asian/Pacific
                                                               4.4%). Within each state, the birth-country composi-
Islanders, in large part because of the high proportion
                                                               tion often varies. In 2003, the most common birth
of foreign-born persons in this population. Among
                                                               country for reported foreign-born TB patients from
foreign-born persons, non-Hispanic blacks had the
                                                               California and Texas was Mexico; for New York, it
highest case rate in 2003 and were the only group
                                                               was China; for Florida, it was Haiti; and for New
with an increase in case rate from 1998 to 2003. In
                                                               Jersey, it was India. In addition, TB patients from
2003, among TB patients born in the United States,
                                                               certain countries were concentrated in certain states.
case rates for non-Hispanic blacks and for American
                                                               For example, in 2003, New York reported 63.5% of
Indian/Alaska Natives were 7.7 and 6.8 times, respec-
                                                               the national total of TB patients born in the Do-
tively, that of non-Hispanic whites. Local, state, and
                                                               minican Republic and 55.7% of those born in Ecua-
federal public health partners, including the CDC
                                                               dor. Florida reported 60.0% of the TB patients born
and the ACET, are collaborating to develop effective
                                                               in Cuba and 49.2% of those born in Haiti; Califor-
strategies to reduce racial disparities in TB [39].
                                                               nia reported 52.0% of the TB patients born in the
                                                               Philippines and 48.6% of the patients born in Laos;
Foreign-born tuberculosis patients                             and Minnesota reported 55.2% of TB patients born
                                                               in Somalia. This diversity poses unique challenges to
    National TB surveillance for patient country of            state and local TB control programs and must be
birth began in 1986, when 4925 (21.8%) new cases               addressed to facilitate case finding and contact in-
were reported among foreign-born persons. The pro-             vestigations and to ensure completion of therapy.
Table 1

                                                                                                                                                                                               epidemiology of tuberculosis in the united states
Number and rate per 100,000 population of tuberculosis cases in the United States in 1998 and 2003
                                      US-born                                            Foreign-born                                     Totalb
                                      1998              2003                             1998             2003                            1998               2003
                                                                         % change                                          % change                                            % change
Race/ethnicitya                       No.       Rate    No.      Rate    1998 – 2003     No.      Rate    No.     Rate     1998 – 2003    No.        Rate    No.       Rate    1998 – 2003
Hispanic                                1282      6.6   1015      4.3    À33.8           2785     26.0    3073    19.6     À24.7            4091     13.5      4115    10.5    À22.2
  Black                                 4968    16.0    3086      9.2    À42.6            841     48.5    1048    52.0         7.2          5816     17.8      4145    11.7    À34.4
  Asian/Pacific Islanderc                 213    5.8     204      5.4     À6.9           3411     55.4    3288    41.2     À25.6            3637     36.9      3510    29.8    À19.3
     Asian                            ...        ...     155      4.4    ...             ...      ...     3252    41.1     ...            ...         ...      3425    30.0    ...
     Native Hawaiian and Other        ...        ...      49     15.7    ...             ...      ...       36    48.6     ...            ...         ...        85    22.1    ...
       Pacific Islander
  White                                3914      2.1    2358      1.2    À40.6            550      8.5     427     6.1     À27.7            4473      2.3      2790      1.4   À38.6
  American Indian/Alaska Native          248    12.6     173      8.1    À36.3           ...      ...     ...     ...      ...               254     12.7       176      8.1   À36.2
Totald                                10,633     4.3    6903      2.7    À38.2           7598     30.2    7902    23.6     À21.8          18,287      6.8    14,874      5.1   À24.4
      In 2003, two modifications were made to the tuberculosis report form: (1) multiple race entries were allowed, with 0.3% selecting more than one race, and (2) the previous category of
Asian/Pacific Islander was divided into ‘‘Asian’’ and ‘‘Native Hawaiian or Other Pacific Islander.’’
      Persons included for whom country of birth was unknown: 56 in 1998 and 69 in 2003.
      For comparison with 1998, data for 2003 Asian/Pacific Islander = Asian plus Native Hawaiian and Other Pacific Islander.
      Persons included for whom race/ethnicity was unknown: 16 for all, 8 for US-born, and 5 for foreign-born persons in 1998; 101 for all, 58 for US-born, and 35 for foreign-born
persons in 2003. In 2003, persons included who selected multiple races: 37 for all, 9 for US-born, 28 for foreign-born persons.

188                                                    schneider et al

                    Number of Foreign-born                                       Percentage of Foreign-born
                    TB Cases                                                     TB Cases
                     10,000                                                                          60

                       8,000                                                                         50

                       2,000                                                                         10

                           0                                                                         0
                               1986    1988   1990    1992    1994    1996    1998   2000   2002
                         Number of Foreign-born TB Cases              Percentage of Foreign-born TB Cases

           Fig. 2. Trends in tuberculosis cases in foreign-born persons in the United States from 1986 to 2003.

    Most TB cases among foreign-born persons are                      requirements for persons seeking permanent resi-
caused by Mycobacterium tuberculosis complex in-                      dency in the United States [43].
fections acquired abroad [41]. Among foreign-born                         TB among foreign-born persons is a major com-
children, aged younger than 15 years, who had TB,                     ponent of TB morbidity in the United States [40]
60% were diagnosed within 18 months of arrival in                     and reflects the global TB situation, defined in 1993
the United States [38]. Prompt evaluation of foreign-                 by the World Health Organization (WHO) as a
born persons for TB following their arrival in the                    global emergency [44,45]. The WHO estimated that
United States can help identify persons who have                      in 2002 there were 8.8 million new cases of TB
LTBI and are eligible for preventive therapy; prompt                  (141 cases per 100,000 population) [46]. Among the
evaluation can prevent development of active TB                       22 high-burden countries, India and China ac-
disease [41,42]. Foreign-born TB patients are also                    counted for 46% of the total. Among the 15 coun-
more likely to have drug resistance and are less likely               tries that have the highest TB rates (>400 cases per
to be HIV infected than US-born TB patients [40].                     100,000 population), 13 are in Africa, and 12 of
The lower proportion of foreign-born TB patients                      these had high TB/HIV incidence rates (>100 cases
infected with HIV results in part from HIV screening                  per 100,000 population) among adults 15 to 49 years

                    Number of US-born                                                 Percentage of US-born
                    TB Cases                                                          TB Cases
                      20,000                                                                              100
                      10,000                                                                              50
                            0                                                                             0
                                1986   1988    1990    1992    1994    1996    1998    2000   2002
                                 Number of US-born TB Cases              Percentage of US-born TB Cases

               Fig. 3. Trends in tuberculosis cases in persons born in the United States from 1986 to 2003.
                                                               epidemiology of tuberculosis in the united states                                                      189

                    Number of states with ≥50% TB cases

                         in foreign-born persons
                                                                                                                                               22          22
                                                                                                                             15          15

                                                          10                                                      9
                                                                                            4    4
                                                                           3     3
                                                                2     2               2
                                                               1986       1988       1990       1992       1994       1996        1998        2000        2002

Fig. 4. Number of states with 50% or more of tuberculosis cases in foreign-born persons in the United States from 1986 to 2003.

old, highlighting the magnitude of the TB/HIV epi-                                                           Drug-resistant tuberculosis
demic and the influence of HIV/AIDS on TB [46].
Therefore, immigration from regions that have high                                                               Drug-resistant TB, especially MDR-TB, places
rates of drug-resistant TB (eg, Eastern Europe) as                                                           an increased burden on all aspects of TB control,
well as from regions that have high rates of HIV in-                                                         including diagnosis, case management, treatment,
fection (eg, sub-Saharan Africa) substantially affect the                                                    and cost [52 – 54]. MDR-TB is defined as resistance
epidemiology of TB in the United States. The CDC                                                             to at least isoniazid and rifampin, two of the most
is collaborating with partners such as the US Agency                                                         effective antituberculosis agents in the TB arsenal.
for International Development, the International                                                             When used in conjunction with other antitubercu-
Union Against TB and Lung Disease (IUATLD), the                                                              losis agents, rifampin can significantly shorten the
KNCV TB Foundation (formerly the Royal Nether-                                                               treatment course of TB. Although many factors
lands Tuberculosis Association), and WHO to assist                                                           have been associated with the development of drug
countries that have high burdens of TB. Collabora-                                                           resistance, including naturally occurring spontaneous
tions have focused on building program capacity,                                                             mutations, two of the most commonly encountered
operational research, and programmatic evaluation to                                                         and preventable factors are nonadherence to therapy
address problems such as TB/HIV and drug resis-                                                              and inappropriate use of antituberculosis drugs. Poor
tance in TB patients. TB screening among immigrant                                                           infection-control practices within hospitals caring
and refugee visa applicants is being improved through                                                        for patients who have drug-resistant TB have also
the development of new diagnostic tools [47] and                                                             played an important role in the nosocomial trans-
updated medical screening guidelines [43]. In addi-                                                          mission of MDR-TB [20 – 22].
tion, because Mexico contributes the largest number                                                              Collection of drug-susceptibility results became
of foreign-born TB patients in the United States,                                                            part of routine national TB surveillance in 1993, in
the CDC has been collaborating with partners in the                                                          part because of the recommendations outlined by
United States and Mexico to help control TB along                                                            the National Action Plan to Combat MDR-TB [31].
the United States – Mexico border. These efforts in-                                                         Before 1993, several regional and national drug sus-
clude an innovative new initiative that uses a bina-                                                         ceptibility surveys on TB patients were conducted
tional health card to track and manage binational                                                            [52]. In 1991, findings of a nationwide survey re-
TB patients who cross the border to ensure continuity                                                        vealed 14.2% of cases were resistant to at least one
of TB care and completion of treatment [48,49].                                                              drug and 3.5% were resistant to at least isoniazid
    Worldwide, TB is a recognized cause of morbidity                                                         and rifampin (MDR-TB) [55]. The strongest risk
and mortality in children. A renewed interest by                                                             factor for drug resistance was geographic location.
domestic and international health agencies has                                                               New York City had the highest MDR-TB rate (13%)
focused on mobilizing and strengthening global                                                               and accounted for 61% of the total MDR-TB cases
efforts to improve surveillance, and to promote                                                              reported in the United States.
program and research initiatives to reduce the bur-                                                              Analysis of national TB surveillance data col-
den of TB on children [50,51].                                                                               lected from 1993 through 1996 revealed a 13.5%,
190                                                schneider et al

incidence of resistance to at least one drug, and the          at least isoniazid and 0.9% had MDR-TB. Addition-
incidence of MDR-TB was 2.2% [56]. Higher drug-                ally, drug resistance (MDR-TB and resistance to at
resistance rates were seen among TB patients who               least isoniazid) has been seen more commonly in
have had a previous episode of TB, foreign-born                foreign-born TB patients (2003: MDR-TB, 1.2%;
persons, HIV-infected persons, and persons residing            isoniazid, 10.6%) than in US-born TB patients (2003:
in specific geographic areas (eg, New York City).              MDR-TB, 0.6%; isoniazid, 4.6%).
In the mid-to-late 1990s, several outbreaks involv-                Knowledge of drug-resistance rates worldwide
ing highly drug-resistant strains of M. tuberculosis           is critical to controlling the global epidemic and has
(ie, strain W) were investigated [57 – 59]. These              direct implications for TB control in the United States
strains share a common drug resistance to first-line           [60,61]. A more comprehensive understanding of
antituberculosis medications (eg, isoniazid, rifampin,         global drug resistance was made possible with the
ethambutol, and, at that time, streptomycin) as well           formation of the Supranational Reference Labora-
as resistance to some second-line medications, mak-            tory Network in 1994 and the WHO/IUATLD Global
ing treatment difficult and costly. The majority of            Project on Anti-Tuberculosis Drug Resistance Sur-
strain W TB cases were reported by New York City               veillance. Newly released data reveal that TB patients
[57,59], although outbreaks have occurred elsewhere,           in parts of Eastern Europe and Central Asia are
including one that was attributed to bronchoscope              10 times more likely to have MDR-TB than patients
contamination in South Carolina [58]. To facilitate            in the rest of the world, with some MDR-TB inci-
early detection of strain W isolates, the CDC began            dence rates higher than 10% (Israel, 14.2%; Kazakh-
recommending that health departments notify the                stan,14.2%; Tomsk Oblast [Russian Federation],
CDC of all M. tuberculosis isolates that have                  13.7%; Uzbekistan, 13.2%; Estonia, 12.2%; and
strain W – resistance patterns [59].                           Liaoning [China], 10.4%) [61].
    Since 1998, overall multidrug resistance among
culture-positive TB patients, who do not have a prior          Tuberculosis/HIV coinfection
history of TB, has been relatively stable (~1%)
(Fig. 5), although outbreaks and regional differ-                  Today, any discussion about TB is incomplete
ences continue to occur. Historically, overall drug-           without a discussion about HIV/AIDS. Knowing a
resistance rates among those who have a previous               TB patient’s HIV status is critical to management,
history of TB have been higher than for those who              treatment, contact investigation, and prevention
do not have a previous history of TB. In 2003,                 [62 – 67]. The CDC recommends that all TB patients,
among TB patients who had a prior history of TB,               independent of risk factors, should undergo voluntary
12.6% had resistance to at least isoniazid and 3.6%            HIV counseling, testing, and referral [64,65,67].
had MDR-TB, whereas 7.9% of TB patients who                    Nonetheless, HIV status is not reported nationally
did not have a prior history of TB had resistance to           for many TB patients in the United States. This in-

                     Number of MDR TB Cases                             Percentage of MDR TB Cases
                       450                                                                      3.0
                       300                                                                      2.0
                       150                                                                      1.0
                         0                                                                      0.0
                             1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003
                                 Number of MDR TB Cases            Percentage of MDR TB Cases

Fig. 5. MDR-TB among persons without a history of tuberculosis in the United States from 1993 to 2003. MDR-TB is defined
as resistance to at least isoniazid and rifampin.
                             epidemiology of tuberculosis in the united states                                191

complete reporting of HIV status probably reflects         mented in HIV-infected patients who have low CD4+
several factors including concerns about confiden-         T-lymphocyte counts, extrapulmonary disease, and
tiality, interpretation of laws and regulations in cer-    concomitant antifungal therapy [74,75]. Clinicians
tain states and local jurisdictions, and reluctance by     treating TB-HIV – coinfected persons should be fa-
health care providers to report HIV test results to the    miliar with current diagnostic, management (eg, DOT),
TB surveillance program staff [10]. Information on         and treatment modalities to maximize therapeutic
HIV status was added to the national TB surveillance       success and minimize TB transmission, drug resis-
system in 1993, in response to the TB resurgence.          tance, adverse effects, and treatment failures [64,67].
HIV test results (ie, negative, positive, or indeter-          Globally, the HIV/AIDS epidemic has had an
minate) were reported for 45.7% of TB patients aged        immense impact on TB control, especially in sub-
25 to 44 years in 1993 and for 65.3% in 2002. In           Saharan Africa, where an estimated two thirds of
this group, positive HIV test results were reported for    persons who have HIV/AIDS live, and has contrib-
29.1% in 1993 and for 15.9% in 2002. Historically,         uted significantly to TB morbidity and mortality
reported TB/HIV coinfection rates and case numbers         [76 – 78]. In these countries, TB incidence and case
have been relatively high in a few states and urban        fatality are strongly associated with HIV prevalence.
areas. In 2002, 60% of the positive HIV test results       The prevalence of drug-resistant TB is expected to
among TB patients aged 25 to 44 years were reported        increase greatly as the HIV epidemic spreads to areas
from five areas: California, Florida, Georgia, New         of the world where drug-resistant TB is more
York City, and Texas. Crossmatching of state TB            prevalent (eg, Asia, Eastern Europe) [61,76]. The
registries and HIV/AIDS registries in 1993 and 1994        scaling up of treatment programs providing anti-
revealed that 14% (range, 0% – 31%) of persons             retroviral therapy will require patient and health care
reported to have TB in the United States were also         provider education and close monitoring to opti-
listed in HIV/AIDS registries [68]. TB-AIDS cases          mize therapy, reduce transmission, and reduce drug-
were more likely to be in persons aged 25 to 44 years,     resistant TB [79].
male, culture-positive for M. tuberculosis, and US-
born. In geographic areas where the prevalence rates       Development of new tools
of HIV-infected persons were high, drug resistance,
especially MDR-TB (6%) and rifampin monoresis-                 An important component of disease control is the
tance (3%), was reported among TB-AIDS patients.           development of new diagnostic tests, pharmacologic
    HIV coinfection has several key implications for       agents, and vaccines. The resurgence of TB in the
the overall treatment and management of TB. HIV            mid-to-late 1980s to 1992 was associated with delays
infection increases the risk of (1) TB disease pro-        in the diagnosis and identification of drug resistance.
gression among persons who have LTBI, (2) rapid            This situation generated renewed interest in the de-
progression of those newly infected with M. tuber-         velopment of several new diagnostic tools and the
culosis to active TB disease, and (3) reinfection with     subsequent genomic sequencing of M. tuberculosis.
M. tuberculosis [67,69]. Many of the TB outbreaks          During the past few years, TB diagnostic capabili-
among persons infected with HIV that occurred              ties have improved through new techniques for
during the resurgence were complicated by high             the rapid detection of M. tuberculosis complex (eg,
drug-resistance rates and resulted in mortality rates      nucleic acid amplification tests) [80], identification
reaching 70% [21 – 23]. TB outbreaks among HIV-            of M. tuberculosis (eg, nucleic acid probe), rapid de-
infected persons have illustrated the continued need       tection of latent TB infection (eg, whole-blood inter-
for appropriate treatment and monitoring of this           feron gamma assay [QuantiFERON (Cellestis Inc.,
population [70 – 73]. The use of antiretroviral ther-      Valencia, California)]) [81,82], the investigational
apy has significantly decreased mortality and mor-         enzyme-linked immunospot test (ELISPOT) [83],
bidity, including the development of opportunistic         and differentiation of M. tuberculosis strains (eg,
infections (eg, TB) among HIV-infected persons.            DNA fingerprinting) [84,85].
New concerns have developed, however, concern-                 In the 1990s, molecular genetic typing (genotyp-
ing the potential for drug – drug interactions, develop-   ing) of M. tuberculosis strains became a commonly
ment of resistance to rifamycin, and paradoxical           used tool to understand outbreaks and transmission
reactions. Drug – drug interactions, primarily between     dynamics. In 1996, the CDC established the National
rifamycin and protease inhibitors and nonnucleoside        TB Genotyping and Surveillance Network to deter-
reverse transcriptase inhibitors, have resulted in new     mine the usefulness of molecular genotyping in more
treatment guidelines and recommendations [66,66a].         routine TB control settings using the IS6110-based
Acquired rifampin monoresistance has been docu-            restriction fragment length polymorphism (RFLP)
192                                               schneider et al

technique supplemented with spacer oligonucleotide          1992, with case numbers increasing by 20%. Follow-
typing (spoligotyping) on M. tuberculosis isolates          ing an intensive campaign and mobilization of new
[86,87]. Genotyping, in conjunction with epidemio-          resources, TB cases once again began to decline.
logic investigation, has proven a useful adjunct to         Remarkable gains have been made since the early
epidemiologic investigations in tracing the chain of        1990s, with efforts being concentrated on maintain-
transmission [88]. The techniques are particularly          ing control of TB, speeding the decline of TB, and
useful in outbreaks and institutional settings, identi-     developing new tools [37]. Key TB epidemiologic
fying groups at risk for TB (eg, homeless persons),         features that have been identified include an increas-
identifying contacts and social networks, under-            ing proportion of TB cases among persons born in
standing exogenous reinfection, and confirming labo-        countries where TB is endemic, racial and ethnic
ratory cross-contamination [89,90]. To refine the           disparities, and localized unique epidemiologic pro-
understanding of TB transmission and epidemiol-             files in areas throughout the United States. Develop-
ogy and to advance TB control, the CDC has                  ment of new tools, such as vaccines, antituberculosis
launched the National TB Genotyping Program,                drugs, and rapid diagnostic tests have also been
which provides the capacity to genotype M. tuber-           identified as vital measures needed to eliminate TB
culosis isolates from all culture-positive TB patients      in the United States.
in the United States. Two polymerase chain reaction –           The smallest decline since the resurgence was
based genotyping tests (spoligotyping, mycobacterial        seen in 2003, raising the concern about a possible
interspersed repetitive units analysis) will be supple-     slowing of the progress against TB or even a reversal
mented with IS6110 RFLP testing for selected speci-         of the decline. Despite increasing health care costs
mens [91]. The goal of this program is to improve           and demands for increased programmatic and opera-
the characterization of TB transmission dynamics and        tional efforts, funding for TB control has not in-
to use the results to improve the efficiency of public      creased [95]. The elimination of TB in the United
health interventions.                                       States will require sustained efforts such as identify-
    In 1995, following a several-year hiatus in the         ing and targeting populations at high risk for TB,
USPHS-sponsored clinical trials, the CDC reinstated         remaining actively involved in the global effort
clinical TB research, creating the TB Trials Con-           against TB, and maintaining adequate resources.
sortium (TBTC). The TBTC currently is coordinat-
ing several studies, including efficacy trials for the
use of moxifloxcin as a first-line drug in the treat-       Acknowledgments
ment of TB disease. Information gained from the
earliest of these studies contributed to the Food and          The authors thank the state and local tuberculosis
Drug Administration licensure of rifapentine, a long-       control officials in health departments throughout
acting rifampin and the first anti-TB drug approved         the United States who collected and reported the
in 25 years [92]. Additional studies include a com-         national surveillance data presented in this article,
parison of several generations of QuantiFERON               the surveillance staff at the Division of TB Elimi-
with the tuberculin skin test in the diagnosis of LTBI      nation, Centers for Disease Control and Prevention,
[81]. In 2001, the CDC established the TB Epide-            who maintain the database, Ann H. Lanner for her
miologic Studies Consortium to conduct multicenter          editorial review of the manuscript, and Dr. Thomas
epidemiologic, behavioral, and operational research         Navin and Dr. Michael Iademarco for their critical
studies. Furthermore, recognizing the need for TB           review of the manuscript.
prevention globally, a renewed interest, fueled by
generous funding has resulted in actively revisiting
vaccine development [93,94]. Numerous organiza-             References
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