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 a Division of Tuberculosis and Elimination, Centers for Disease Control and Prevention, 1600 Clifton Road, MS E-10, Atlanta, GA 30333, USA b 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 . in urban settings, and partly owing to the natural The need to expand data collection to include TB behavior of epidemics . 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 . 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: firstname.lastname@example.org (E. Schneider). TB for surveillance purposes became paramount , 0272-5231/05/$ – see front matter. Published by Elsevier Inc. doi:10.1016/j.ccm.2005.02.007 chestmed.theclinics.com 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 . 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 . 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 . 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 . 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 . 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 . 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 28,000 Number of TB Cases 26,000 24,000 22,000 20,000 18,000 16,000 14,000 12,000 1981 1983 1985 1987 1989 1991 1993 1995 1997 1999 2001 2003 Year 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 . 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  such as correctional facilities  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 . 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 . 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 . 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 . The 2003 TB rate among all foreign-born . 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 . 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, Race/ethnicity 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 . 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 Non-Hispanic 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 a 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.’’ b Persons included for whom country of birth was unknown: 56 in 1998 and 69 in 2003. c For comparison with 1998, data for 2003 Asian/Pacific Islander = Asian plus Native Hawaiian and Other Pacific Islander. d 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. 187 188 schneider et al Number of Foreign-born Percentage of Foreign-born TB Cases TB Cases 10,000 60 8,000 50 40 6,000 30 4,000 20 2,000 10 0 0 1986 1988 1990 1992 1994 1996 1998 2000 2002 Year 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 . fections acquired abroad . 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  60% were diagnosed within 18 months of arrival in and reflects the global TB situation, defined in 1993 the United States . 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) . 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 . 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 90 80 15,000 70 60 10,000 50 40 30 5,000 20 10 0 0 1986 1988 1990 1992 1994 1996 1998 2000 2002 Year 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 30 in foreign-born persons 25 23 22 22 20 15 15 14 10 10 9 6 5 4 4 3 3 2 2 2 0 1986 1988 1990 1992 1994 1996 1998 2000 2002 Year 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 . 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  and played an important role in the nosocomial trans- updated medical screening guidelines . 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 . 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 . 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) . 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% . 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 . 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 . Liaoning [China], 10.4%) . 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 3.0 400 350 300 2.0 250 200 150 1.0 100 50 0 0.0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 Year 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 . 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 . TB-AIDS cases mize therapy, reduce transmission, and reduce drug- were more likely to be in persons aged 25 to 44 years, resistant TB . 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) , 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) , 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 . The techniques are particularly ing control of TB, speeding the decline of TB, and useful in outbreaks and institutional settings, identi- developing new tools . 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 . 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 . 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 . 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, . 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. 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